Phil. Trans. R. Soc.

B (2007) 362, 1585–1599

doi:10.1098/rstb.2007.2054
Published online 11 April 2007

Cortical mechanisms of action selection:

the affordance competition hypothesis
Paul Cisek*
Department of physiology, University of Montréal, C.P. 6128 Succursale Centre-ville, Montréal,
Quebec, H3C 3J7 Canada
At every moment, the natural world presents animals with two fundamental pragmatic problems:
selection between actions that are currently possible and specification of the parameters or metrics of
those actions. It is commonly suggested that the brain addresses these by first constructing
representations of the world on which to build knowledge and make a decision, and then by computing
and executing an action plan. However, neurophysiological data argue against this serial viewpoint. In
contrast, it is proposed here that the brain processes sensory information to specify, in parallel, several
potential actions that are currently available. These potential actions compete against each other for
further processing, while information is collected to bias this competition until a single response is
selected. The hypothesis suggests that the dorsal visual system specifies actions which compete against
each other within the fronto-parietal cortex, while a variety of biasing influences are provided by
prefrontal regions and the basal ganglia. A computational model is described, which illustrates how this
competition may take place in the cerebral cortex. Simulations of the model capture qualitative
features of neurophysiological data and reproduce various behavioural phenomena.
Keywords: decision making; action selection; cerebral cortex; computational modelling

1. INTRODUCTION Traditional cognitive theories propose that these two

At every moment, the natural environment presents questions are resolved in a serial manner, so that we
animals with many opportunities and demands for select ‘what to do’ before specifying ‘how to do it’.
action. The presence of food offers an opportunity to According to this view, the perceptual system first
satiate hunger, while the appearance of a predator collects sensory information to build an internal
demands caution or evasion. An animal cannot per- descriptive representation of objects in the external
form all these behaviours at the same time because they world (Marr 1982). Next, this information is used
often share the same effectors (you only have two along with representations of current needs and
hands; you can only transport yourself in one direction memories of past experience to make judgments and
at a time, etc.). Thus, one fundamental issue faced by decide upon a course of action ( Newell & Simon 1972;
every behaving creature is the question of action Johnson-Laird 1988; Shafir & Tversky 1995). The
selection. This question must be resolved, in part, by resulting plan is then used to generate a desired
using external sensory information about objects in the trajectory for movement, which is finally realized
world and, in part, by using internal information about through muscular contraction (Miller et al. 1960;
the current behavioural needs. Keele 1968). In other words, the brain first builds
Furthermore, the animal must tailor the actions it knowledge about the world using representations
performs to the environment in which it is situated. which are independent of actions, and this knowledge
Grasping a fruit requires accurate guidance of the hand is later used to make decisions, compute an action plan
to the location of the fruit, while evading a predator and finally execute a movement.
requires one to move in an unobstructed direction that However, studies on the cerebral cortex have encoun-
leads away from the threat. The specification of the tered difficulties in interpreting neural activity in terms of
parameters of actions is a second fundamental issue distinct perceptual, cognitive or motor systems. For
faced by behaving creatures. Specification of actions example, visual processing diverges in the cortex into
also must use sensory information from the environ- separate systems sensitive to object identity and spatial
ment. In particular, it requires information about the location (Ungerleider & Mishkin 1982), with no single
representation of the world (Stein 1992), leading to the
spatial relationships among objects and surfaces in the
question of how these disparate systems are bound
world, represented in a coordinate frame relative to
together to form a unified percept (von der Malsburg
the orientation and configuration of the animal’s body.
1996; Cisek & Turgeon 1999). Cells in the posterior
parietal cortex appear to reflect a mixture of sensory
*[email protected] (Andersen 1995; Colby & Goldberg 1999), motor
Electronic supplementary material is available at http://dx.doi.org/10. (Snyder et al. 1997) and cognitive information (Platt &
1098/rstb.2007.2054 or via http://www.journals.royalsoc.ac.uk. Glimcher 1999), leading to persistent debates on their
One contribution of 15 to a Theme Issue ‘Modelling natural action functional role. A recent review of data on the parietal
selection’. cortex has suggested that ‘current hypotheses concerning

1585 This journal is q 2007 The Royal Society

1586 P. Cisek Affordance competition hypothesis

parietal function may not be the actual dimensions along neurophysiological data than the traditional framework
which the parietal lobes are functionally organized; on of cognitive psychology (Cisek 2001).
this view, what we are lacking is a conceptual advance that Continuous interaction with the world often does
leads us to test better hypotheses’ (Culham & Kanwisher not allow one to stop to think or to collect information
2001, pp. 159–160). In other words, perhaps the and build a complete knowledge of one’s surroundings.
concepts of separate perceptual, cognitive and motor To survive in a hostile environment, one must be ready
systems, which theoretical neuroscience inherits from to act at short notice, releasing into execution actions
cognitive psychology, are not appropriate for bridging that are at least partially prepared. These are the
neural data with behaviour. fundamental demands which shaped brain evolution.
Even stronger concerns regarding cognitive psychol- They motivate animals to process sensory information
ogy’s suitability as a bridging framework are raised by in an action-dependent manner to build represen-
considerations of evolutionary history (Sterelny 1989; tations of the potential actions which the environment
Hendriks-Jansen 1996). Brain evolution is strikingly currently affords. In other words, the perception of a
conservative and major features of modern neural given natural setting may involve not only represen-
organization can be seen in the humble Haikouichthys, a tations which capture information about the identity of
primitive jawless fish that lived during the Early objects in the setting, but also representations which
Cambrian epoch over 520 Myr ago (Shu et al. 2003). specify the parameters of possible actions that can be
Since the development of the telencephalon, the basic taken (Gibson 1979; Fadiga et al. 2000; Cisek 2001).
outline of the vertebrate nervous system has been With a set of such potential actions partially specified,
strongly conserved throughout its phylogenetic history the animal is ready to quickly perform actions if
(Butler & Hodos 1996; Holland & Holland 1999; Katz & circumstances demand. In essence, it is possible that
Harris-Warrick 1999) and even recently, elaborated the nervous system addresses the questions of specifi-
structures such as the mammalian neocortex have cation (how to do it) before performing selection (what
homologues among non-mammalian species (Medina & to do). Indeed, for continuous interactive behaviour, it
Reiner 2000). Although the idea that brain evolution may be best to perform both specification and selection
consists of new structures being added on top of old processes at all times to enable continuous adjustment
structures (e.g. the ‘Triune Brain’; MacLean 1973) is to the changing world.
still popular among non-specialists, it has been rejected The proposal made here is that the processes of action
in recent decades of comparative neuroanatomical selection and specification occur simultaneously and
work (Deacon 1990; Butler & Hodos 1996). Brain continue even during overt performance of move-
evolution consists of the differentiation and special- ments. That is, sensory information arriving from the
ization of existing structures through shifts in existing world is continuously used to specify several currently
axonal projection patterns (Deacon 1990; Krubitzer & available potential actions, while other kinds of
Kaas 2005), not through the addition of new information are collected to select from among these
structures. Thus, the basic anatomical and functional the one that will be released into overt execution at a
organization of the primate brain reflects an ancient given moment (Kalaska et al. 1998; Kim & Shadlen
architecture which was well established by the time of 1999; Cisek 2001; Glimcher 2001; Gold & Shadlen
the earliest terrestrial tetrapods. This architecture 2001; Platt 2002; Cisek & Kalaska 2005). From this
could not have been designed to serve the needs of perspective, behaviour is viewed as a constant compe-
higher cognitive abilities, which did not exist, but must tition between internal representations of the potential
have been laid down so as to best address the needs of actions which Gibson (1979) termed ‘affordances’.
simple interactive behaviour. Hence, the framework presented here is called the
An emphasis on the brain’s role in interactive ‘affordance competition hypothesis’.
behaviour is by no means novel. Similar ideas have for a It is not proposed that complete action plans are
long time been central to theories in ethology (Hinde prepared for all of the possible actions that one might take
1966; Ewert et al. 2001) and have recently led to several at a given moment. First, only actions which are currently
viewpoints on cognition (Adams & Mele 1989; Clark available are specified in this manner. Second, many
1997; Beer 2000; Núñez & Freeman 2000; Thelen possible actions are eliminated from processing by
et al. 2001) and interactive behaviour (Brooks 1991; selective attention mechanisms which limit the sensory
Hendriks-Jansen 1996; Prescott et al. 1999; Seth 2007). information that is transformed into representations of
All these are similar to several lines of thought that are action. Finally, complete action planning is not proposed
much older (Mead 1938; Merleau-Ponty 1945; Ashby even for the final selected action. Even in cases of highly
1965; Powers 1973; Gibson 1979; Maturana & Varela practised behaviours, no complete pre-planned motor
1980) in some cases by over a hundred years (Jackson programme or entire desired trajectory appears to be
1884; Bergson 1896; Dewey 1896). Most of these prepared (Kalaska et al. 1998; Cisek 2005).
viewpoints emphasize the pragmatic aspects of
behaviour (Piaget 1967; Gibson 1979; Millikan 1989),
a theme that underlies several proposals regarding 2. THE AFFORDANCE COMPETITION
representation (Dretske 1981; Gallese 2000; Hommel HYPOTHESIS
et al. 2001), memory (Ballard et al. 1995; Glenberg 1997) The view of behaviour as a competition between
and visual consciousness (O’Regan & Noë 2001). Here, actions has been common in studies on animal
it is proposed that these views, which emphasize behaviour and the interpretation of subcortical circuits
the brain’s role in controlling behaviour in real time (Ewert 1997; Prescott et al. 1999; Ewert et al. 2001).
(Cisek 1999), provide a better basis for interpreting However, it is more rarely used to explain the activity of

Phil. Trans. R. Soc. B (2007)

 Affordance competition hypothesis P. Cisek 1587

prem
otor c
ex ortex
l cort potential actions
eta
pari

attention cognitive
decision making

prefrontal
eam

cortex
al str

basal
predicted ganglia behavioural
dors

feedback biasing

ventral stre
am

object specification
identity
cer
ebe temporal selection
llum
cortex

visual feedback motor

command

Figure 1. Sketch of the proposed neural substrates of the affordance competition hypothesis, in the context of visually guided
movement. The primate brain is shown, emphasizing the cerebral cortex, cerebellum and basal ganglia. Filled dark arrows
represent processes of action specification, which begin in the visual cortex and proceed rightward across the parietal lobe,
transforming visual information into representations of potential actions. Polygons represent three neural populations along this
route: the leftmost represents the encoding of potential visual targets, modulated by attentional selection; the middle represents
potential actions encoded in parietal cortex; and the rightmost represents activity in premotor regions. Each population is
depicted as a map of neural activity, with activity peaks corresponding to the lightest regions. As the action specification occurs
across the fronto-parietal cortex, distinct potential actions compete for further processing. This competition is biased by input
from the basal ganglia and prefrontal cortical regions which collect information for action selection (double-line arrows). This
biasing influences the competition in a number of loci, and owing to reciprocal connectivity, these influences are reflected over a
large portion of the cerebral cortex. The final selected action is released into execution and causes both overt feedback through
the environment (dashed black arrow) and internal predictive feedback through the cerebellum.

cerebral cortical regions, perhaps, owing to an assump- intraparietal (LIP) area is concerned with the control of
tion that the cortex is a new structure concerned with gaze (Snyder et al. 1997), represents space in a body-
new cognitive functions. However, as discussed above, centred reference frame (Snyder et al. 1998a,b) and is
this assumption is not justified. The organization of the strongly interconnected with parts of the oculomotor
cerebral cortex has been conserved for a long time, system including the frontal eye fields (FEFs) and the
motivating one to interpret it, like subcortical circuits, superior colliculus (Paré & Wurtz 2001). In contrast,
in terms of interactive behaviour. Figure 1 outlines a the medial intraparietal (MIP) area is involved in arm
proposal on how the affordance competition hypothesis reaching actions ( Ferraina & Bianchi 1994; Kalaska &
may be used to interpret neural data from the primate Crammond 1995; Snyder et al. 1997), represents target
cerebral cortex during visually guided behaviour. locations with respect to the current hand location
The visual system is organized into two parallel (Graziano et al. 2000; Buneo et al. 2002) and is
processing pathways: an occipito-temporal ‘ventral interconnected with frontal regions involved in reach-
stream’, in which cells are sensitive to information ing, such as the dorsal premotor cortex (PMd; Johnson
about the identity of objects, and an occipito-parietal et al. 1996; Marconi et al. 2001).
‘dorsal stream’, in which cells are sensitive to spatial These observations are consistent with the proposal
information (Ungerleider & Mishkin 1982). From the that the major role of the dorsal visual stream is not to
traditional cognitive perspective, the ventral stream build a unified representation of the world, but rather
builds a representation of ‘what’ is in the environment, to mediate various visually guided actions (Goodale &
while the dorsal stream builds a representation of Milner 1992). It may therefore be part of the system for
‘where’ things are. However, the dorsal stream does not action specification ( Fagg & Arbib 1998; Kalaska et al.
appear to contain any unified representation of the 1998; Cisek & Turgeon 1999; Cisek 2001; Passingham &
space around us, but rather diverges into a number of Toni 2001), processing visual information to specify
substreams each specialized towards the needs of potential actions of various kinds: LIP cells specify
different kinds of actions (Stein 1992; Andersen et al. potential saccade targets; MIP cells specify possible
1997; Wise et al. 1997; Colby & Goldberg 1999; directions for reaching, etc. Furthermore, the dorsal
Matelli & Luppino 2001). For example, the lateral stream represents not only a single unique movement

Phil. Trans. R. Soc. B (2007)

1588 P. Cisek Affordance competition hypothesis

that has already been selected, but rather offers a superior colliculus (Basso & Wurtz 1998; Horwitz et al.
variety of options to choose from multiple saccade 2004). Such mixing of variables is difficult to interpret
targets (Platt & Glimcher 1997; Kusunoki et al. 2000) from the perspective of distinctions between sensory,
as well as multiple reaching movements (Cisek et al. motor and cognitive systems, and it has led to persistent
2004). It does not, of course, represent all possible debates about the functional role of specific cortical
movements. As one proceeds along the dorsal stream, regions. For example, some studies have shown that
one finds an increasing influence of attentional neurons in LIP area respond only to stimuli which
modulation, with information from particular regions capture attention, leading to its interpretation as a
of interest enhanced while information from other ‘salience map’ (Colby & Goldberg 1999; Kusunoki
regions is suppressed (Desimone & Duncan 1995; Treue et al. 2000; Bisley & Goldberg 2003). However, other
2001). The result is that the parietal representation of studies have shown that these activities are stronger
external space becomes increasingly sparse as one moves when the stimulus serves as the target of a saccade
away from striate cortex (Gottlieb et al. 1998). In other (as opposed to a reach), leading to the interpretation of
words, only the most promising targets for movements LIP as a representation of intended saccades (Snyder
make it so far to be represented in the parietal cortex. et al. 1997, 1998a,b, 2000). These competing interpre-
From this perspective, the phenomenon of selective tations have been the subject of a long and vibrant
attention is seen as an early mechanism for action debate. However, from the perspective of the affor-
selection (Allport 1987; Neumann 1990; Tipper et al. dance competition hypothesis, both interpretations are
1992, 1998), reducing the volume of information that is correct: neural activity in fronto-parietal regions
transformed into action-related representations. correlates with sensory and motor variables because it
As mentioned, parietal cortical areas are strongly and is involved in the specification of potential actions using
reciprocally interconnected with frontal regions involved sensory information, and it is modulated by decision
in movement control. LIP is interconnected with FEF, variables (including salience/attention) because a
MIP with PMd and primary motor cortex (M1), AIP competition between potential actions is influenced
with ventral premotor cortex (PMv), etc. (Matelli & by various sources of biasing inputs.
Luppino 2001). As a result, the fronto-parietal system There are many potential sources from which biasing
may be viewed as a set of loops spanning over the central inputs might originate. Since action selection is a
sulcus, each processing information related to a different fundamental problem faced by even the most primitive
aspect of movement (Pandya & Kuypers 1969; Jones
of vertebrates, it probably involves neural structures
et al. 1978; Marconi et al. 2001). If these regions are
which developed very early and have been conserved in
involved in representing potential actions, as assumed
evolution. A promising candidate is the basal ganglia
here, then they appear to do so in tandem. For example,
(Mink 1996; Kalivas & Nakamura 1999; Redgrave et al.
potential reaching actions are represented together by
1999; Frank et al. 2007; Hazy et al. 2007), which are
both MIP and PMd (Cisek et al. 2004; Cisek & Kalaska
strongly interconnected with specific cortical areas
2005). It is proposed that the competition between
(Alexander & Crutcher 1990a; Middleton & Strick
potential actions plays out in large part within this
2000) and exhibit activity that is related to both
reciprocally interconnected fronto-parietal system.
Within each cortical area, cells with different movement movement parameters (Alexander & Crutcher 1990b,c)
preferences mutually inhibit each other, creating a and decision variables such as reward (Schultz et al. 2000)
competition between distinct potential actions. This and expectation (Lauwereyns et al. 2002). However, it is
competition is biased by excitatory input from a variety of also probable that action selection involves brain
sources, including both cortical and subcortical regions. structures which have become particularly developed in
The influence of all these biasing factors modulates the recent evolution, such as the PFC of primates. The PFC
activity in frontal and parietal neurons, with information is strongly implicated in decision making (Bechara et al.
favouring a given action causing activity related to that 1998; Kim & Shadlen 1999; Fuster et al. 2000; Miller
action to increase, while information against an action 2000; Rowe et al. 2000; Tanji & Hoshi 2001), which may
causes it to decrease. be viewed as an aspect of advanced action selection.
Indeed, neurophysiological evidence for the modu- Neurons in the dorsolateral prefrontal cortex (DLPFC)
lation of fronto-parietal activity by ‘decision factors’ is are sensitive to various combinations of stimulus features,
very strong. For example, recent studies on decision and this sensitivity is always related to the particular
making show that LIP activity correlates not only with demands of the task at hand (di Pellegrino & Wise 1991;
sensory and motor variables, but also with decision Hoshi et al. 1998; Rainer et al. 1998; Kim & Shadlen
variables such as expected utility (Platt & Glimcher 1999; Quintana & Fuster 1999). Prefrontal decisions
1999), local income (Sugrue et al. 2004), hazard rate appear to evolve through the collection of ‘votes’ for
( Janssen & Shadlen 2005) and relative subjective categorically selecting one action over others, as demon-
desirability (Dorris & Glimcher 2004). More generally, strated by studies of saccade target and reach target
variables traditionally considered as sensory, cognitive selection (Kim & Shadlen 1999; Tanji & Hoshi 2001). Of
or motor appear to be mixed in the activity of individual course, the PFC is not a homogeneous system but a
cells in many regions, including prefrontal cortex diverse collection of specialized regions, including some
(PFC; Hoshi et al. 2000; Constantinidis et al. 2001), which appear to be involved in the aspects of working
premotor cortex (Romo et al. 2004; Cisek & Kalaska memory (Fuster & Alexander 1971; Bechara et al. 1998;
2005), FEF (Thompson et al. 1996; Gold & Shadlen Petrides 2000; Rowe et al. 2000). Here, we include only a
2000; Coe et al. 2002), LIP (Platt & Glimcher 1997; very simplified account of one particular subregion of
Shadlen & Newsome 2001; Coe et al. 2002) and the PFC, the DLPFC.

Phil. Trans. R. Soc. B (2007)

 Affordance competition hypothesis P. Cisek 1589

What role might the ventral visual stream play within (a) visual input
the functional architecture of figure 1? Cell responses in
anterior inferotemporal (IT) cortex are sensitive to the
features of a currently viewed stimulus (Desimone et al.
1984; Tanaka et al. 1991), and to the behavioural PPC PFC
R B
context in which this stimulus is presented (Eskandar
et al. 1992). These results have been taken to implicate
IT in object recognition. However, it may also serve a
more humble role. Studies on animal behaviour over PMd1
the last hundred years have shown that many kinds of PMd2
behaviours are elicited by simple combinations of
PMd3
particular stimulus features, which ethologists referred
GO
to as ‘sign stimuli’ ( Tinbergen 1950; Hinde 1966).
Neural responses in IT cortex are compatible with a M1
putative role in sign stimulus detection, which could
serve as a front-end input to action selection via direct motor output
projections from temporal cortex to prefrontal regions
(Saleem et al. 2000). Thus, an early role of what is now (b)
the ventral stream may have been the detection of the

cell activity
stimulus combinations that were relevant for selection (i)
of actions in a particular behavioural context, and this
may have eventually evolved into the sophisticated
object recognition ability of modern mammals.
(ii)

cell activity
3. A COMPUTATIONAL MODEL
OF REACHING DECISIONS
The broad concepts outlined in §2 can be translated
into more concrete and testable hypotheses through a preferred azimuth
mathematical model of the neural processes which may
Figure 2. Computational model. (a) Each neural layer is
implement action specification and selection in the depicted by a set of circles representing cells with different
mammalian cerebral cortex. A model of the cortical preferences for a movement parameter (e.g. direction). Thin
mechanisms which specify reaching movements and arrows represent topographic connections (in most cases
select between them has been described by Cisek reciprocal) between layers involved in action specification.
(2006) and is summarized briefly here (see also the Grey polygons represent the input to and from prefrontal
electronic supplementary material). cortex, which is divided into two subpopulations each
Figure 2a illustrates the circuit model and suggests preferring a different stimulus colour. These projections are
how its elements may correspond to specific cortical also topographic, but with much lower spatial resolution (see
regions. Since the model focuses on visually guided electronic supplemental material). Visual inputs are pre-
sented to the input layer, and the GO signal gates activity in
reaching actions, it includes some of the main cortical
primary motor cortex. Abbreviations: PPC, posterior parietal
regions involved in reaching behaviour, such as the cortex; PFC, prefrontal cortex; PMd, dorsal premotor
posterior parietal cortex (PPC), dorsal premotor cortex; M1, primary motor cortex. (b) Each population
cortex ( PMd), primary motor cortex (M1) and consists of cells with different preferred directions, and their
prefrontal cortex (PFC). These were chosen as a pattern of activity can represent (i) one potential reach
subset of the complete distributed circuits for reaching direction or (ii) several potential directions simultaneously.
control, sufficient to demonstrate a few central
concepts. Other relevant regions not currently mod- with similar tuning excite each other, while neurons
elled are the supplementary motor areas, somatosen- with dissimilar tuning inhibit each other. Between
sory cortex and many subcortical structures including populations, neurons with similar tuning excite each
the basal ganglia, red nucleus, etc. The input to the other through reciprocal topological connections.
model consists of visual information about target Noise is added to all neural activities. For details of
direction and a signal triggering movement onset the model’s implementation, see the electronic supple-
(GO signal), and the output is the direction of mentary material.
movement. The control of the overt movement is not In the model, neural populations do not encode a
simulated here (for compatible models of execution, unique value of a movement parameter (such as a single
see Bullock & Grossberg 1988; Houk et al. 1993; direction in space), but can represent an entire
Kettner et al. 1993; McIntyre & Bizzi 1993; Bullock distribution of potential values of movement par-
et al. 1998; Cisek et al. 1998). ameters (e.g. many possible directions represented
In the model, each neural population was simultaneously). This proposal is related to the
implemented as a set of 90 mean-rate leaky-integrator attention model of Tipper et al. (2000), the ‘decision
neurons, each of which is broadly tuned to a particular field’ theory of Erlhagen & Schöner (2002) and the
direction of movement. All the weights are fixed to ‘Bayesian coding’ hypothesis (Dayan & Abbott 2001;
resemble the known anatomical connections between Sanger 2003; Knill & Pouget 2004). It suggests that
the modelled regions. Within each population, neurons given a population of cells, each with a preferred value

Phil. Trans. R. Soc. B (2007)

1590 P. Cisek Affordance competition hypothesis

of a particular movement parameter, one can interpret Finally, the model suggests that the competition
the activity across the population as something akin to a which occurs between potential actions represented in
probability density function of potential values of that the fronto-parietal system is biased by a variety of
parameter. Sometimes, the population may encode a influences from other regions, including the basal
range of contiguous values defining a single action, and ganglia (Redgrave et al. 1999) and PFC (Miller 2000;
at other times, several distinct and mutually exclusive Tanji & Hoshi 2001) which accumulate evidence for
potential actions can be represented simultaneously as each particular choice (figure 1). Here, only the
distinct peaks of activity in the population (figure 2b). influence of PFC is modelled, although it is probable
The strength of the activity associated with a particular that basal ganglia projections play a significant role in
value of the parameter reflects the likelihood that the action selection ( Frank et al. 2007; Houk et al. 2007).
final action will have that value and is influenced by a Several studies have shown that some cells in lateral
variety of factors including salience, expected reward, prefrontal cortex (PFC) are sensitive to conjunctions of
estimates of probability, etc. This hypothesis predicts relevant sensory and cognitive information (Rainer
that activity in the population is correlated with many et al. 1998; White & Wise 1999; Miller 2000; Tanji &
decision variables, as observed in frontal (Kim & Hoshi 2001), and that they gradually accumulate
Shadlen 1999; Gold & Shadlen 2000; Hoshi et al. evidence over time (Kim & Shadlen 1999). Many
2000; Coe et al. 2002; Roesch & Olson 2004; Romo studies have suggested that orbitofrontal cortex and the
et al. 2004) and parietal cortices (Platt & Glimcher basal ganglia provide signals which predict the reward
1999; Shadlen & Newsome 2001; Coe et al. 2002; associated with a given response (Schultz et al. 2000),
Glimcher 2003; Dorris & Glimcher 2004; Sugrue et al. which could also serve as input to bias the fronto-
2004; Janssen & Shadlen 2005). parietal competition.
The model suggests that sensory information in the The operation of the model can be most easily
dorsal visual stream is used to specify the spatial understood in the context of a particular task. For
parameters of several currently available potential example, figure 3a shows a reach-decision task in which
actions in parallel. These potential actions are rep- the correct target was indicated through a sequence of
resented simultaneously in frontal and parietal cortical cues: during the spatial-cue (SC) period, two possible
regions, appearing as distinct peaks of activity in the targets were presented, and during a subsequent
neural populations involved in sensorimotor processing colour-cue (CC) period, one of these was designated
(Platt & Glimcher 1997; Cisek et al. 2004; Cisek & as the correct target. In the model, the appearance of
Kalaska 2005; figure 2b). Whenever multiple peaks the spatial cue causes activity in two groups of cells in
appear simultaneously within a single frontal or parietal PPC, each tuned to one of the targets. Mutual
cortical region, they compete against each other excitation between nearby cells creates distinct peaks
through mutual inhibition. This is related to the biased of activity, which compete against each other through
competition mechanism in theories of visual attention the inhibitory interactions between cells with different
(Desimone 1998; Boynton 2005). To state it briefly, preferred directions. Owing to the topographic pro-
cells with similar parameter preferences excite each jections between PPC and PMd, two peaks appear in
other, while cells with different preferences inhibit each PMd as well, although they are weaker in the lower
other. This basic mechanism can explain a variety of PMd layers (compare layers PMd1 and PMd3). These
neural phenomena such as the inverse relationship two peaks continue to be active and compete against
between the number of options and neural activity each other even after the targets vanish, owing to the
associated with each (Basso & Wurtz 1998; Cisek & positive feedback between layers. At the same time,
Kalaska 2005), narrowing of tuning functions with activity accumulates in the PFC cells selective for the
multiple options (Cisek & Kalaska 2005) and relative particular location–colour conjunctions. The colour
coding of decision variables (Roesch & Olson 2004). cue is simulated as uniform excitation to all PFC cells
Since neural activities are noisy, competition between preferring the given colour (in this case, PFCR), and it
distinct peaks of activity cannot follow a simple ‘winner- pushes this group of PFC cells towards stronger activity
take-all’ rule, or random fluctuations would determine than the other. This causes the competition in PMd to
the winner each time, rendering informed decision become unbalanced, and one peak increases its activity
making impossible. To prevent this, small differences in while the other is suppressed. In the model, this is
the levels of activity should be ignored by the system. equivalent to a decision. Finally, once the GO signal is
However, if activity associated with a given choice given, activity is allowed to flow from PMd3 into M1
becomes sufficiently strong, then it should be allowed and the peak of the M1 activity is taken to define the
to suppress its opponents and conclusively win the initial direction of the movement.
competition. In other words, there should be a threshold The simulation reproduces many features of neural
of activity above which a particular peak is selected as activity recorded from the dorsal premotor and primary
the final response choice. This is consistent with motor cortex of a monkey performing the same reach-
sequential sampling models of decision making decision task (Cisek & Kalaska 2005). As shown in
(Usher & McClelland 2001; Mazurek et al. 2003; figure 3a, PMd cells tuned to both spatial targets were
Reddi et al. 2003; Smith & Ratcliff 2004; Bogacz et al. active during the SC, and then during the CC, one of
2007) which propose that decisions are made when these became more strongly active (predicting the
neural activity reaches some threshold. In the model, this monkey’s choice), while the other was suppressed.
threshold emerges from the nonlinear dynamics between Note how the activity was weaker while both options
competing populations of cells (Grossberg 1973; Cisek were present, consistent with the hypothesis that the
2006; see electronic supplementary material). two groups of cells exert an inhibitory influence on

Phil. Trans. R. Soc. B (2007)

 Affordance competition hypothesis P. Cisek 1591

(a) (b) (c)

GO GO GO
colour cue colour cue spatial cue
spatial cue spatial cue colour cue
rostral
PMd rostral
PMd
caudal
caudal
neural data

PMd
PMd
M1
GO 0
SC –10 +10
GO 1s GO CC
activity versus baseline (Hz)
PD CC CC
SC SC
time PMd1

PMd3

M1
model simulations

PPC

PFCR

PFCB

GO GO GO
CC 0 2 CC SC
simulated activity SC CC
SC
Figure 3. Comparison between neural activity and model simulations in three kinds of tasks. (a) Two-target task. During the
spatial cue (SC), two possible targets are presented, one red and one blue. During the colour cue (CC), the centre indicates
which of these is the correct target. The GO signal instructs the monkey to begin the movement. Neural data (Cisek & Kalaska
2005) are shown from three sets of neurons: rostral PMd, caudal PMd and primary motor cortex (M1). In each, neural activity is
depicted as a three-dimensional coloured surface in which time runs from left to right and cells are sorted by their preferred
direction along the left edge. Coloured circles indicate the locations of the two targets. Simulated model activities are depicted in
the same format, where black lines indicate behavioural events (spatial cue on, spatial cue off, colour cue on, colour cue off, GO).
(b) One-target task, same format as (a). (c) Matching task, same format as (a).

each other. As in the model, these phenomena were the model, this burst is more correctly described as a
seen more strongly in the rostral part of PMd than in brief representation of a potential action, aborted
the caudal part. The model also exhibits sustained quickly in light of the prior information provided by
activity (‘working memory’) because after the targets the colour cue. Again, this is seen most strongly in the
are removed (second black line in the simulation rostral part of PMd, in both the data and the model.
images), target information is maintained in both In addition to reproducing qualitative features of
PPC and PMd (figure 3a,b). neural activity during the reach-decision tasks of Cisek &
Figure 3c shows a variation of the task in which the Kalaska (2005), the model produces important
CC is presented before the SC. In this case, no psychophysical results on the spatial and temporal
directionally tuned activity appears in PMd during characteristics of human motor decisions. For example,
the CC period, and after the spatial targets are it is well known that reaction times in choice tasks
presented, there is sustained activity corresponding increase with the number of possible choices. This can
only to the correct target. Thus, the neural activity is be explained by the model (figure 4a) because the
determined not by the sensory properties of the activity associated with each option is reduced as the
stimulus (which are the same as in figure 3a), but by number of options is increased (compare model PMd
the movement information specified by the stimulus. activity in figure 3a with figure 3b), and it therefore
However, note that immediately after the SC, there is a takes longer for the activity to reach the decision
brief burst towards the incorrect target, in both the threshold. Furthermore, it has also been shown that
neurons in rostral PMd and in the PMd1 population in reaction time is not only determined by the number
the model (figure 3c). One might be tempted to classify of targets, but also by their spatial configuration.
this as a pure ‘sensory’ response. However, at least in For example, Bock & Eversheim (2000) showed that

Phil. Trans. R. Soc. B (2007)

1592 P. Cisek Affordance competition hypothesis

(a) 200 accumulation to threshold: that with weaker evidence,

reaction time (ms) the rate of accumulation is slower and the threshold is
reached later in time, and therefore variability in
accumulation rate produces broader distributions of
100 reaction times (Carpenter & Williams 1995; Ratcliff
et al. 2003; Smith & Ratcliff 2004).
The model also explains several observations on the
spatial features of movements made in the presence of
multiple choices. For example, Ghez et al. (1997)
1 2 3 4 showed that when subjects are forced to make choices
quickly, they move to targets randomly if they are
(b) 300 spaced farther than 608 apart (‘discrete mode’), and
in-between them if the targets are close together
(‘continuous mode’), as shown in figure 5a. The
reaction time (ms)

200 model reproduces all of these results (figure 5b).

When two targets are far apart, they create multiple
competing peaks of activity in the PMd–PPC popu-
100 lations, and the decision is determined by the peak that
happens to fluctuate higher when the signal to move is
given. However, if the targets are close together, then
0 their two corresponding peaks merge into one owing to
the positive feedback between cells with similar
parameter preferences (a similar explanation has been
(c) proposed by Erlhagen & Schöner 2002). In a related
40 experiment, Favilla (1997) demonstrated that the
percentage of latencies

M = 1.00
discrete and continuous modes can occur at the same
30 M = 0.625 time when four targets are grouped into two pairs that
are far apart, but each of which consists of two targets
20
close together (figure 5c). This is also reproduced by
10 the model (figure 5d; except for an additional central
bias exhibited by human subjects). With four targets,
peaks corresponding to targets within each pair merge
0 200 400 600 together and then the two resulting peaks compete and
latency of decision (ms) are selected discretely.
Figure 4. Latency effects. (a) Simulated reaction time during
tasks with one, two, three or four targets presented for 1.3 s,
followed by a single correct target for 0.1 s, followed by the 4. DISCUSSION
GO signal. Reaction times were calculated as first time after This paper describes a theoretical framework called the
the GO signal that any neuron in the M1 population exceeded ‘affordance competition hypothesis’, which suggests
an activity threshold of 1.5. The mean and standard error are that behaviour involves a constant competition
shown for NZ300 replications in each condition. between currently available opportunities and demands
(b) Simulated reaction time when cues are presented for for action. It is based on the idea that the brain’s basic
0.8 s followed by a single target for 0.3 s prior to the GO. The functional architecture evolved to mediate real-time
bars show meanGs.e. of reaction time in four conditions:
interaction with the world, which requires animals to
when three cues are presented 808 apart, two cues 1608 apart,
two cues 808 apart or no cue at all. NZ100 in each condition.
continuously specify potential actions and to select
(c) Distributions of decision latency computed during between them. This framework is used to interpret
simulations (each with two targets) using a CC cue of neural data from the primate cerebral cortex,
different magnitudes. The decision latency was calculated as suggesting explanations for a number of important
the time between the CC cue and the first time any PMd3 cell neurophysiological phenomena. A computational
activity exceeded 0.75. NZ200 for each condition. model is presented to illustrate the basic ideas of the
hypothesis and suggest how neural populations in the
reaction time in a reaching task is similar with two or cerebral cortex may implement a competition between
five targets as long as they subtend the same spatial representations of potential actions.
angle, but shorter if two targets are closer together. The mathematical model presented above shares a
This finding is difficult to account for with models in number of features with existing models of decision
which the options are represented by discrete groups of making. For example, it is similar to a class of models
neurons, but is easily reproduced in a model such as the called ‘sequential sampling models’ (Roe et al. 2001;
present one, in which movements are specified by a Usher & McClelland 2001; Mazurek et al. 2003; Reddi
continuous population (figure 4b). The model also et al. 2003; Smith & Ratcliff 2004), which propose that
reproduces the important finding that reducing the decisions are made by accumulating information for a
quality of evidence for a given choice makes reaction given choice until it reaches some threshold. In some
times longer and more broadly distributed. The model models, the evidence is accumulated by a single process
produces this (figure 4c) through the same mechanism (e.g. Smith & Ratcliff 2004), in some it is collected by
proposed by other models which involve a gradual separate processes which independently race towards

Phil. Trans. R. Soc. B (2007)

 Affordance competition hypothesis P. Cisek 1593

(a) (c)
SR ≤ 80 81–200 ms >200 ms SR < 100 ms
40
percentage of responses
10

targets
close
20

15 40

targets
far
20

0
–40 +40 response direction (deg.) response direction (deg.)

(b) (d )
SR = 50 ms SR = 200 ms SR = 500 ms SR = 50 ms
20 20
percentage of responses

targets
close
10 10

20 20

targets
far
10 10

0 0
location of first M1 peak location of first M1 peak

Figure 5. Data and simulation of the timed response paradigms of Favilla (1997) and Ghez et al. (1997). (a) Behavioural data
from the Ghez et al. (1997) task. Each panel shows the distribution of initial directions of force production with respect to two
targets (vertical lines). Data are aligned such that the correct target (solid line) is on the right. Different distributions are reported
for different delays between target identification and movement onset, and for different angular separations between the targets.
(b) Simulations of the Ghez et al. (1997) task. Each panel shows the distribution of initial directions, calculated as the preferred
direction of the first M1 cell whose activity exceeded a threshold of 1.75. (c) Behavioural data from Favilla (1997) task, in which
four targets are shown either all 308 apart or grouped into two pairs that are far apart. Same format as (a). (d ) Simulations of
Favilla (1997) task, same format as (b). SR, time between selection and response.

the threshold (Roe et al. 2001; Reddi et al. 2003), and The model presented here makes a number of
in some the independent accumulators inhibit each predictions which distinguish it from many other
other (Usher & McClelland 2001; Bogacz et al. 2007). models of decision making. First, it focuses on
Some models separate the decision process into serial decisions about actions (as opposed to sensory
stages (e.g. Mazurek et al. 2003) and in some it occurs discrimination) and suggests that these are made within
when a single population exhibits a transition from the very same neural circuits that control the execution
biased competition to binary choice ( Wang 2002; of those actions. These circuits are distributed among a
Machens et al. 2005). While the present model shares large set of brain regions. In the case of visually guided
similarities with these, it extends their scope in an reaching, decisions are made within the fronto-parietal
important way. In all of the models of decision making circuit that includes both PMd and parietal area MIP.
described above, the choices are predefined and In the specific mathematical formulation described
represented by distinct populations, one per choice. above, the competition between actions uses infor-
In contrast, the present model suggests that the choices mation from PFC, but the decision first appears in
themselves emerge within a population of cells whose PMd, in agreement with data (Wallis & Miller 2003).
activity represents the probability density function of However, the broader framework of the affordance
potential movements. In other words, the model competition hypothesis does not impose any rigid
describes the mechanism by which the choices are temporal sequence in which decisions appear in the
defined using spatial information. In this sense, it is fronto-parietal system. Each population in the network
related to the models of Tipper et al. (2000) and is proposed to involve competitive interactions, and
Erlhagen & Schöner (2002), which also discuss biasing influences can modulate this competition in
continuous specification of movement parameters different places. Since cortico–cortical connections are
within a distributed representation. To summarize, bidirectional, if a decision begins to emerge in one
the present model may be seen as combining three lines region, then it will propagate outward to other regions.
of thought: (i) sequential sampling models of accumu- For example, decisions based on sensory features such
lation of evidence to a threshold, (ii) models of a phase as stimulus salience may first appear in parietal cortex
transition from encoding options to binary choice and then influence frontal activity. In contrast,
behaviour (see electronic supplementary material), decisions based on abstract rules may first be expressed
and (iii) models of action specification within a in frontal regions and propagate backward to PPC.
distributed population. It also suggests a plausible Thus, decisions are proposed to emerge as a ‘dis-
manner in which these concepts can be used to tributed consensus’, which is reached when a compe-
interpret neural data in specific cortical regions. tition between representations of potential actions is

Phil. Trans. R. Soc. B (2007)

1594 P. Cisek Affordance competition hypothesis

brain function
(a)

perception cognition action

olfaction attention planning

audition vision working decision forward inverse
memory making models kinematics
colour object propositional trajectory
vision vision recognition spatial
of space logic generation
memory

brain function
(b)

action action
specification selection

decision
grasping reaching running attention affect
making

forward vision of inverse arm sign stimulus action

arm models nearby space kinematics detection sequencing

spatial object propositional

memory recognition logic

Figure 6. Two possible conceptual taxonomies of neural processes. (a) The taxonomy implied by classical cognitive science, in
which brain functions are classified as belonging to perceptual, cognitive or action systems. (b) An alternative taxonomy, in
which brain functions are classified as processes aiding either action specification or action selection.

unbalanced by the accumulation of evidence in favour competition between actions (Kornblum et al. 1990;
of a given choice. Hendriks-Jansen 1996; Toates 1998; Prescott et al.
Although the mathematical model presented here is 1999; Ewert et al. 2001), and as discussed above, to a
similar in some ways to previous models of decision number of philosophical proposals made throughout
making, it is based on a somewhat unusual theoretical the last hundred years. The present discussion is an
foundation. The affordance competition hypothesis, attempt to unify these and related ideas with a growing
illustrated schematically in figure 1, differs in several body of neurophysiological data. It is suggested that a
important ways from the cognitive neuroscience frame- great deal of neural activity in the cerebral cortex can be
works within which models of decision making are interpreted from the perspective of a competition
usually developed. Importantly, it lacks the traditional between potential movements more easily than in
emphasis on explicit representations which capture terms of traditional distinctions between perception,
knowledge about the world. For example, the activity in cognition and action (Cisek 2001). It is not suggested
the dorsal stream and the fronto-parietal system is not that distinctions between perceptual, cognitive and
proposed to encode a representation of objects in motor processes be discarded entirely (they are
space, or a representation of motor plans, or cognitive certainly appropriate for interpreting primary sensory
variables such as expected value. Instead, it implements and motor regions), but only that other conceptual
a particular, functionally motivated mixture of all of distinctions may be better suited to understanding
these variables. From a traditional perspective, such central regions.
activity appears surprising because it does not have any Figure 6 provides a schematic of the conceptual
of the expected properties of a sensory, cognitive or differences between the affordance competition
motor representation. It does not capture knowledge hypothesis and the traditional frameworks of cognitive
about the world in the explicit descriptive sense neuroscience. Traditional frameworks tend to view
expected from cognitive theories and has proven brain function as consisting of three basic classes of
difficult to interpret from that perspective (see above). neural processes (figure 6a): perceptual systems, which
However, from the perspective of affordance compe- take sensory information and construct internal
tition, mixtures of sensory information with motor representations of the world (e.g. Marr 1982); cognitive
plans and cognitive biases make perfect sense. Their systems, which use that representation along with
functional role is not to describe the world, but to memories of past experience to build knowledge,
mediate adaptive interaction with the world. form judgments and make decisions about the world
In summary, instead of viewing the functional (Newell & Simon 1972; Johnson-Laird 1988; Shafir &
architecture of behaviour as serial stages of represen- Tversky 1995); and action systems, which implement
tation, we view it as a set of competing sensorimotor the decisions through planning and execution of
loops. This is by no means a novel proposal. It is related movements (Miller et al. 1960; Keele 1968). Each of
to several theories which describe behaviour as a these broad classes can be subdivided into subclasses.

Phil. Trans. R. Soc. B (2007)

 Affordance competition hypothesis P. Cisek 1595

For example, perception includes different modalities endow organisms with the ability to interact with their
such as vision, which can be subdivided further into environment in adaptive ways.
object recognition, spatial vision, etc. Likewise, cogni-
The author wishes to thank Andrea Green and Steve Wise
tion includes processes such as working memory for their helpful comments on various versions of this
storage and retrieval, decision making, etc. These manuscript. This work was supported by the New Emerging
conceptual classes and subclasses are used to define Teams grant NET-54000 from the Canadian Institutes of
research specialities, categorize scientific journals and Health Research and a Discovery Grant from the Natural
interpret the functional role of specific brain regions. Sciences and Engineering Research Council of Canada.
Here, a different taxonomy of concepts is proposed
(figure 6b). Brain function is seen as fundamentally
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