626

Population coding and behavioral choice William B Kristan Jr* and Brian K Shawl

Many individual behavioral acts are produced by the The idea of motor commands being coded by population combined activity of large populations of broadly tuned activity is not new. For example, neuronal schemes for , and the neuronal populations for different behaviors population coding of movements have been proposed for can overlap. Recent experiments monitoring and manipulating saccadic eye movements [S], arm movements [6], bending neuronal activity during behavioral decisions have begun in leeches [7], and orientation in insects [S]. However, to shed light on the mechanisms that enable overlapping each of these cases consists of singular behaviors with one populations of neurons to generate choices between parameter-the direction of movement-varying over a categorically distinct behaviors. continuous range of movements. The issue we address here is whether the term ‘population coding’ can also be applied when the motor outputs are categorically distinct Addresses behaviors, rather than continuously varying responses. We ‘Biology Department, University of California at San Diego, 9500 Gilman Drive, La Jolla, California 92093-0357, USA; will not attempt to address this issue definitively, but will e-mail: [email protected] review results that bear on it in the hope of fueling (and tThe Institute, 10640 John Jay Hopkins Drive, San constraining) further discussion and debate. Diego, California 92121, USA; e-mail: [email protected]

Current Opinion in Neurobiology 1997, 7:826-831 Behavioral choice also contains cognitive aspects, as exemplified by discussions of this topic in two different http:llbiomednet.comlelecreflO959438800700826 reviews in a recent issue of Current Opinion in Neurobi- 0 Current Biology Ltd ISSN 0959-4388 ology on Cognitive [9,10]. This review will

Abbreviations complement, rather than reiterate, the issues discussed in LIP lateral intraparietal (area) those reviews. MT middle temporal (area) STG stomatogastric ganglion The neural basis of behavioral choice: the classical view Perhaps the most influential scheme for how the behav- ioral repertoire of an animal is organized in the nervous Introduction system was proposed by Tinbergen [ 11.A modified version To behave adaptively, an animal must be able to choose of this scheme is presented in Figure 1, in which neural the appropriate behavior for its current circumstances and ‘centers’ are arrayed in a hierarchy, with the highest must coordinate the various behaviors in its repertoire. levels concerned with more abstract behavioral functions Proposals for how nervous systems might implement such (i.e. drives) and lower levels with more specific aspects decision-making processes date back to classical of motor output (in modern terminology, these would be [l-3]. With a small number of exceptions, however, it is central pattern generators, motor pools, etc.). At a middle only recently that the neural mechanisms that underlie level are centers that control particular whole-animal behavioral choice have come under experimental scrutiny. behaviors, with each center dedicated to the production of that behavior. In this model, the basis for choices between Here, we review some recent work that has begun to behaviors is mutual inhibition between the centers at shed light on how nervous systems produce choices the same level, although Tinbergen recognized that between behaviors, focusing on papers published over there could be other, more complex neural mechanisms the past year. A recurring theme to be found in this involved. work is the suggestion that single neurons can contribute to multiple behaviors (i.e. they are ‘multiplexed’) and, In the ensuing decades, the discovery of neurons that because individual neurons respond to a broad class could, when stimulated, single-handedly initiate whole- of stimuli (i.e. they are ‘coarsely coded’), that large animal behaviors in invertebrates [ll], and the discovery populations of neurons may act to determine what in vertebrates of discrete nuclei that could do the same action an animal takes. In fact, these two concepts are [12], seemed to fit nicely with this hierarchical scheme. often discussed under the general notion of ‘distributed These ‘command-like’ neurons or systems appeared well processing’ [4]. Coarse coding and multiplexing represent suited to fill the role of the behavior-dedicated centers a challenge to classical proposals for the neural basis proposed by Tinbergen (see (131). This view received of decision-making (described below) and suggest the further support from reports of a number of examples possibility that categorically distinct behavioral outcomes of inhibition between command-like neurons [14,15]. A may be coded by the profile of activity across a population simple model also provided support: a simulation em- of neurons, any one of which could contribute to multiple ploying mutually inhibitory connections among command behaviors. neurons for several different behaviors was able to produce Population coding and behavioral choice Kristan and Shaw 827

Cir.*-r 4 ray”,= I on the behavior, it may be driven by reflex pathways or a central pattern generator, and may play either a critically important role or a modest one.

Another example is provided by our study of the choice Level of the between swimming and shortening in the medicinal major (reproductive) leech [ZO”]. We found that most of the command-like neurons of the swim circuit, which can elicit swimming 2nd level when artificially stimulated, were excited by stimuli that (fighting, nesting, etc.) produced shortening, as well as by stimuli that produced swimming (Figure 2). Only one of the command-like neurons, cell 204, was inhibited during shortening. These 3rd level results raise the possibility that most of the cells (consummatory act) previously identified as command-like components of the swim circuit are, in fact, multifunctional neurons that 4th level (fins) contribute to more than one behavior. While inhibition is probably important for the choice between swimming 5th level and shortening, this inhibition is not targeted to all (fin rays) command-like neurons, nor exclusively to command-like neurons. 6th level (muscles) 5’ B A conclusion to be drawn from these two studies 7th level 3 6 (motor units) [ 19**,20**] is that neurons with command-like properties 8 2 need not act as behavior-dedicated decision points. To express this another way, knowing what a single command- like cell is doing will not necessarily allow one to predict A hierarchical scheme proposed by Tinbergen Ill, based largely what the animal is doing. If CC5 is active, for instance, upon ethological studies, to explain the nature of decision-making a sea hare may be turning its head, or undergoing local in animals. He proposed that animals make high-level decisions first (e.g. whether to reproduce or to feed), then make a sequence of withdrawal, or performing some other behavior [18’,19”]. more and more specific decisions, down to the level of the choice of If cell Trl is active, a leech may be about to swim or specific motor patterns. In this scheme, decisions are made at ‘nodes’ about to shorten [ZO”] (Figure 2). As a further example in the brain, represented by circles in the diagram. Once activated, of the complex roles that such cells may play, stimulating a node inactivates all the other nodes at the same level, either by inhibiting them directly or by removing their excitation from the higher a particular high-level interneuron in the leech, cell TX, level. Modified from [l]. can produce swimming in a quiescent or terminate an ongoing swimming bout [Zl]. a variety of surprisingly complex and life-like behavioral Overlapping sets of neurons can be activated sequences (161. In a more complex modeling effort, during categorically distinct behaviors however, a more distributed use of sensory information One consequence of using population coding for contin- over many hierarchical layers, rather than a process of uous behaviors is that the same will be active mutual inhibition at each level, produced more advanta- during a number of different responses (Figure 3). Recent geous behavioral choices [ 171. Recent neurophysiological work shows that this can also be true for categorically investigations also suggest that behavioral choices involve distinct, incompatible behaviors. In one example already complex interactions among neuronal populations. We will considered (Figure Z), many interneurons initially iden- now review some of the points raised by this work. tified as part of the leech swim circuit are also active during shortening [ZO”]. In an additional example, most Higher-order neurons need not be dedicated neurons in the Ap!ysia abdominal ganglion fire during to single behaviors the performance of two or three different behaviors: the An implication of the scheme of Figure 1 is that each gill withdrawal reflex, spontaneous gill contractions, and command-like neuronal system should be dedicated to the respiratory pumping [ZZ]. Another system with extensive production of a single behavior. A number of recent studies neuronal overlap is the spinal circuitry generating the have shown that this is not always the case. For instance, turtle scratch reflex. Turtles show three categorically CCS, an identified neuron in Ap&sia that is both sufficient different forms of scratching, each having a distinct and necessary for the arterial shortening component of mechanosensory . A set of propriospinal a local withdrawal response [18*], also contributes to interneurons contribute to generating two forms of the five other behaviors [19”]. These behaviors are diverse, scratch, the rostra1 and pocket forms. When tested, most ranging from withdrawal to locomotion to feeding. The of these interneurons show broad tuning, responding to cell plays different roles in different behaviors: depending stimulation of both the rostra1 and pocket fields [23]. 828 Motor systems

Figure 2

Parallel Swim-activating shortening .“Frl neurons interneurons /- e..mm.mC..,i m / Q ‘command-like’ cells Swim-gating neurons

Swim oscrllator neurons

Interneurons

Motor neurons

Actrve during swimming Active for both Active dunng shortening 0 Inhibited during shortening 0 swrmming and shortening lnhibrted during swrmmrng

-0 lnhibrtory connection I Excrtatory connection

Activity patterns during swimming and shortening in neurons previously identified either as part of the swim circuit or as part of the shortening circuit in the medicinal leech. The swim circuit is organized hierarchically and contains three interneuronal levels: the swim-activating cells, the gating cells, and the oscillator cells [21]. The shortening circuit includes the S cell and other, parallel, interneuronal pathways [40]. The neurons are active in one of three ways: only during swimming (inhibited during shortening), during both behaviors, or during shortening (inhibited during swimming) [20”,40-421. For clarity, the only synaptic connections shown within the swim circuit are those known to link adjacent functional levels. The parallel shortening interneurons and their connections are shown as dotted outlines because their cell bodies have not been identified [401. Note that during shortening, cells 204 and 208 receive competing excitatory and inhibitory inputs, and that the inhibitory influences ‘win out’. The S cell is inhibited during swimming episodes [42], but swim-initiating stimuli, such as mechanical stimulation of the posterior region, can transiently excite the S cell. In general, the circles represent segmental neurons that are either singular (204, 206, and S), paired (21, 26, 33, 61, 115, L), or a class of neurons (there are four pairs of dorsal longitudinal muscle excitors [DES] and three pairs of ventral longitudinal muscle excitors NEs]). There is a single pair of each of the swim-activating neurons, Trl and SEl, in the anterior brain.

Thus, stimulation of the rostra1 and pocket receptive fields multiple behaviors may be more common than specialized, excites overlapping populations of spinal interneurons, behavior-dedicated ones. even though the behaviors these stimuli produce fall into two distinct categories. A demonstration of population activity corresponding to a perceptual judgment These examples suggest some degree of overlap in the An extensive series of detailed experiments by Newsome sets of neurons contributing to different behaviors-that and his colleagues (nicely summarized recently [24]j is, some degree of sharing of circuitry may be the concluded that perceptual decisions about the direction rule, even when the behaviors are very different from of motion in a stochastic visual display (as monitored one another. Concomitantly, they suggest that general- by eye movement responses) are made by summing purpose, or ‘multiplexed’ neurons that contribute to the activity of a population of neurons in, among other Population coding and behavioral choice Kristan and Shaw 829

shows that neurons in this area are active before choices are made, and that their activity predicts the direction of movement [29*]. Hence, the decision maker may be located in LIP, or in the connections onto neurons in LIP. pwl A a1 Because of the complexity of the interactions in the visual a2 a3 centers, however, the decision could be made in other a4 brain areas, with the information passed along to LIP. : ove;lap of A and B ‘Neuronal democracies’ and where the votes are tallied If there are distinct ‘decision’ elements, as in Figure 3, how do they make their decision? In other words, who tallies the votes in what has been termed a ‘neuronal democracy’ [30]? Such decision makers must be integration sites where competing signals converge,

Schema for behavioral choice in two populations of neurons and these neurons should fire if and only if a particular representing abstracted sensory information. The pooled signal from behavior ensues. For the case of the decision between each is compared by a population of decision neurons: if a>b, one swimming and shortening in the leech (Figure Z), cell 204 behavior is elicited; if b >a, the alternative behavior is elicited. This is our best candidate for such an integration site [20**,21]: kind of network should be capable of making decisions whether the sensory pools overlap, even extensively, or not at all. Adapted from an array of signals that promote and suppress swimming Figure 2 in [27”1. are directed to cell 204, and the resulting level of activity in cell 204 may determine whether or not the animal will swim. A hallmark of such decision units is that they places, the middle temporal area (area MT) of the would fire strongly only during one specific behavior. monkey’s visual cortex. This conclusion is based upon Examples of such apparently behavior-dedicated neurons correlations observed between area MT cell activity and continue to be discovered. For instance, an interneuron behavioral decisions (25’1, as well as the effects of in Clione can trigger whole-body withdrawal behavior microstimulation in area hlT in influencing decisions when stimulated, is inhibited during feeding (which has [26]. A conceptual model of this kind of decision-making a higher behavioral priority than withdrawal), and, in process is presented in Figure 3 [27**]: the activity within turn, suppresses swimming (which has a lower behavioral two populations of neurons (each with differing response priority than withdrawal) [31*]. In this case, the strategy characteristics) is pooled, this activity is read out at a more appears to be as simple as possible: the inputs, outputs downstream ‘decision’ stage, and the categorical outcome and effects of this neuron mirror the behavioral hierarchy is determined by which population is more active. This of the animal. represents a ‘winner-take-all’ strategy for decision-making. MT microstimulation results provided evidence that Selecting particular motor patterns from perceptual judgments of motion direction do indeed multifunctional networks involve a winner-take-all operation [26]. Interestingly, a Other neuronal mechanisms have been suggested as more recent study using a quite different perceptual-motor substrates for making categorical decisions. For instance, task-tracking of a visual target-concluded that the the stomatogastric ganglion (STG) of crustaceans contain direction of eye movement could be determined by multifunctional neuronal circuits that generate a variety taking a vector average of the preferred direction of each of motor patterns related to chewing and swallowing neuron in area MT, weighted by its firing rate [28**]. food [32], and a variety of neuronal mechanisms have Taken together, these two studies [26,28**] suggest that been documented that select distinctly different motor the pattern of activity in area MT can be read out patterns. The modulatory proctolin neuron (RIPN), which in service of two different strategies-vector averaging projects to the STG, produces a particular pattern of STG or winner-take-all-depending upon the task being activity when it is stimulated by means of its direct effects performed. on the STG and by inhibiting certain other projection neurons [33”]. Another recently identified projection Whatever the coding strategy used, where is the decision neuron produces a distinctly different type of pattern accomplished? The firing of neurons in area MT suggests in the STG [34-l. The suggestion from these studies is that they can provide the information needed to make the that different motor patterns are ‘called up’ by activity decision about movement direction, but that the decision in particular projection neurons or combinations of such itself is made elsewhere [27”]. In the context of Figure 3, neurons. the MT neurons make up the populations that feed into the decision stage, but do not constitute the decision Another apparently multifunctional circuit is the spinal stage itself. Initial recordings from the lateral intraparietal network responsible for producing both swimming and (LIP) cortical area, which receives input from area MT, struggling in Xe~opus embryos [35]. Recent reports show 030 Motor systems

that application of glutamate receptor agonists can elicit References and recommended reading either swimming or struggling, depending on the concen- Papers of particular interest, published within the annual period of review, tration of the agonist [36’], and that direct sensory neuron have been highlighted as: stimulation can elicit either behavior, depending on the . of special interest amount of stimulation [37’]. This supports the hypothesis l * of outstanding interest that the same network produces both behaviors, and 1. Tinbergen N: The Study of Instinct. Oxford: Clarendon Press; suggests that it is simply the level of excitation onto the 1951. network that determines which behavior is expressed. 2. Von Frisch K: The Dance Language and Orientation of Bees. Cambridge, Massachusetts: Belknap; 1967. Conclusions 3. Lorenz K: Foundations of Ethology. Heidelberg: Springer-Verlag; 1981. Looking back at the model proposed by Tinbergen nearly 4. Morton DW, Chiel HJ: Neural architectures for adaptive half a century ago (Figure l), many of the questions about behavior. Trends Neurosci 1994, 17:413-420. the neuronal mechanisms that underlie the making of 5. Sparks DH, Holland R, Guthrie BL: Size and distribution of behavioral choices remain unanswered, but they are now movement fields in the monkey superior colliculus. Brain Res 1976, 113:21-34. more clearly framed. The fact that population codes are used at a number of levels in both simple and complex 6. Georgopoulos AP, Caminiti R, Kalaska JF, Massey JT: Spatial coding of movement: a hypothesis concerning the coding of nervous systems, for both sensory perception and motor movement direction by motor cortical populations. Erp Brain control, does make the interpretation of single-cell data Res 1963, 7(suppl):327-336. more complicated, but it does not significantly change 7. Locker-y SR, Wittenberg G, Kristan WB Jr, Cottrell GW: Function of identified interneurons in the leech elucidated using the nature of the questions that need to be answered. networks trained by back-propagation. Nature 1989, 340:466- Which neurons influence the decision? Where are they 471. located? What neuronal mechanisms are used to make 8. Theunissen FE, Miller JP: Representation of sensory information in the cricket cereal sensory system. II. Information theoretic the decision? It is clear that these questions can be calculation of system accuracy and optimal tuning-curve addressed more directly in simpler animals with fewer widths of four primary interneurons. / Neurophysiol 1991, neurons in their nervous systems and at the sensory and 66:1690-l 703. motor ends of neuronal processing. For instance, one can 9. Beiser DG, Sherwin EH, Houk JC: Network models of the basal ganglia. Curr Opin Neurobiol 1997, 7:165-l 90. imagine a neuronal mechanism for how a frog chooses 10. Duncan J, Humphreys G, Ward R: Competitive brain activity in an appropriate position to grab its prey [38] more readily visual . Gun Opin Neurobiol 1997, 7:255-261. than imagining the neuronal basis for choosing the next 11. Wiersma CAG, lkeda K: Interneurons commanding swimmeret move in a chess game. There are indications, however, movements in the crayfish, Procambarus clarkii (Girard). Comp Biochem Physiol 1964, 12:509-525. that we are beginning to uncover the secrets of even the most complex areas of the brain, somewhere near the 12. Grillner S: Locomotion in vertebrates: central mechanisms and reflex interaction. fhysiol Rev 1975, 55:247-304. sensorimotor watershed. 13. Kupfermann I, Weiss KR: The concept Behav Brain Sci 1976, 1:3-l 0.

Where might we expect progress to be made in finding the 14. Kovac MP, Davis WJ: Neural mechanisms underlying behavioral neuronal mechanisms of decision-making in population choice in Pleurobranchaea. J Neurophysiof 1960, 43:469-467. codes? Because of the complexity of the networks, 15. Krasne FB, Lee SC: Response-dedicated trigger neurons as control points for behavioral actions: selective inhibition of modeling studies should help, both to predict mechanisms lateral giant command neurons during feeding in crayfish. of categorical neuronal circuits [39] and to test whether J Neurosci 1966, 6:3703-3712. proposed mechanisms can work [27”]. Also, because such 16. Edwards DH: Mutual inhibition among neural command decisions are probably made in populations of neurons, systems as a possible mechanism for behavioral choice in crayfish. J Neurosci 1991, 11 :121 O-1 223. functional brain imaging studies may define potential sites 1 7. Tyrrell T: The use of hierarchies for action selection. Adaptive of decision-making. Finally, the comparative approach Behav 1993, 1:367-420. holds great hope. Like a variety of other general systems 16. Xin Y, Weiss KR, Kupfermann I: A pair of identified interneurons concepts (e.g. , command systems and . in Aplysia that are involved in multiple behaviors are necessary central pattern generators), behavioral choice appears to and sufficient for the arterial-shortening component of a local withdrawal reflex. J Neurosci 1996, 16:4516-4526. use common neuronal and network mechanisms across A single, higher-order identified interneuron in Apfysia, cell CC5, IS sufficient many animal phyla. Hence, there is hope that much and necessary for the arterial shortening component of the local tentacular withdrawal response, and the bilateral pair of CC5 neurons may be sufficient can be learned about the neuronal basis of complex and necessary for the arterial shortening component of the head withdrawal choices-whether to go to work or to the beach, response. Hence, this single neuron qualifies as a command neuron for ar- terial shortening, a component of withdrawal responses. whether to save or to invest- by studying the neuronal 19. Xin Y, Weiss KR, Kupfermann I: An identified interneuron mechanisms of more simple choices made by a variety of . . contributes to aspects of six different behaviors in Apfysia. animals. I Neurosci 1996, 165266-5279. This study provides evidence that CC5, shown to play a critical role in arterial shortening in Aplysia [16*1, also contributes to five other distinct behaviors. CC5 receives synaptic inputs during a variety of behaviors, and connects to Acknowledgements motor neurons and interneurons involved in several behaviors. By monitoring ‘fhe wntmg of [his rcvic\r was supported by National Insrirures of Health a neuron targeted by CC5 during each of the behaviors, before and after research grant NS25’9lh (\I% Kn\tan) and the Neurosciences Research eliminating the input from CC5 to this neuron, the authors showed that CC5 1:oundatinn (BK Shan). plays roles of varying importance in the different behaviors. Population coding and behavioral choice Kristan and Shaw 831

20. Shaw BK, Kristan WB: The neuronal basis of the behavioral 30. Heiligenberg W: Neural Nets in E/e&: Fish. Cambridge, . . choice between swimming and shortening in the leech: control Massachusetts: MIT Press; 1991. is not selectively exercised at higher circuit levels. I Neurosci 31. Norekian TP, Satterlie RA: Whole body withdrawal circuit and its 1997, 17:786-795. . involvement in the behavioral hierarchy of the mollusk Clione Swimming and shortening are two incompatible whole-body behaviors per- limacina. J Neurophysiol 1996, 75:529-537. formed by the leech. The neuronal circuit underlying swimming is organized A newly identified set of neurons in Clione, the pleural withdrawal (PI-W) hierarchically and contains three interneuronal levels, including two upper neurons, are sufficient to produce whole-body withdrawal when stimulated. levels of command-like neurons. This study monitored the responses of swim The PI-W cells receive inhibition from neurons involved in feeding behavior, circuit interneurons to mechanosensory stimuli that produced shortening. and, in turn, inhibit neurons involved in swimming. This mirrors the behavioral The majority of the swim circuit neurons, including most of the command-like priority sequence of Clione: feeding dominates whole-body withdrawal, and cells and all neurons at the highest hierarchical level, were excited by stimuli whole-body withdrawal dominates swimming. that produced shortening. Only a subset of neurons, including one of the command-like cells, were inhibited during shortening. 32. Dickinson PS: Interactions among neural networks for behavior. Curr Opm Neurobiol 1995, 5:792-798. 21. Brodfuehrer PD, Debski EA, O’Gara BA, Friesen WO: Neuronal control of leech swimming. I Neurobiol 1995, 27:403-418. 33. Blitz DM, Nusbaum MP: Motor pattern selection via inhibition of . . parallel pathways. J Neurosci 1997, 17:4965-4975. 22. Wu JY, Cohen LB, Falk CX: Neuronal activity during different behaviors in Ap/ysia: a distributed organization? Science 1994, Previous work had shown that stimulation of an identified modulatory pro- jection neuron (MPN), which projects to the stomatogastric ganglion (STG) 263:820-823. of the crab, could elicit a particular pyloric rhythm from the STG. This study 23. Berkowitz A, Stein PS: Activity of descending propriospinal demonstrates that MPN additionally suppresses the gastric mill rhythm, and axons in the turtle hindlimb enlargement during two forms of that it does so by inhiblttng other protection neurons. fictive scratching: broad tuning to regions of the body surface. J Neurosci 1994, 14:5089-5104. 34. Norris BJ, Coleman MJ, Nusbaum MP: Pyloric motor pattern . modification by a newly identified projection neuron in the 24. Newsome VVT: Deciding about motion: linking perception to crab stomatogastric nervous system. J Neurophysiol 1996, action. J Comp Physiol [Al 1997, 181:5-l 2. 75:97-l 08. 25. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA: Describes a newly identified projection neuron in the crab, modulatory com- . A relationship between behavioral choice and the visual missural neuron 5 (MCN5). This neuron elicits a distinct and unique pyloric responses of neurons in macaque MT. Visual Neurosci 1996, rhythm in the stomatogastric ganglion (STG) when stimulated. 13:87-l 00. 35. Soffe SR: Two distinct rhythmic motor patterns are driven by Single-cell recordings were made in the middle temporal area (MT) of mon- common premotor and motor neurons in a simple vertebrate keys while they performed a forced-choice visual discrimination task. A trial- spinal cord. J Neurosci 1993, 13:4456-4469. to-trial correlation was tested between the monkey’s choice and the activ- ity of single neurons, under conditions in which the stimulus remained the 36. Soffe SR: Motor patterns for two distinct rhythmic behaviors . same. A modest, but significant, correlation was found. The authors argue, evoked by excitatory amino acid agonists in the Xenopus based on the weakness of this relationship for any given neuron and on the embryo spinal cord. J Neurophysiol 1996, 75:1815-l 825. prevalence of the relationship across the group of neurons studied, that large Applying the same glutamate receptor agonists can produce either swim- pools of neurons probably contribute to the behavioral decision. ming or struggling I” the Xenopus embryo, depending on the concentration: lower concentrations cause swimming, higher concentrations cause strug- 26. Salzman CD, Newsome WT: Neural mechanisms for forming a gling. This occurs without activation of the Rohon-Beard sensory neurons, perceptual decision. Science 1994, 264:231-237. disproving an earlier hypothesis that release of a neuromodulator from the 27. Shadlen MN, Britten KH, Newsome WT, Movshon JA: A Rohon-Beard cells is what determines whether swimming or struggling is . . computational analysis of the relationship between neuronal expressed. and behavioral responses to visual motion. J Neurosci 1996, 37. Soffe SR: The pattern of sensory discharge can determine 16:1486-1510. . the motor response in young Xenopus tadpoles. J Comp A modeling study, utilizing the experimental results of [25’] and other stud- Physiol W 1997, 180:71 l-71 5. ies by Newsome and his colleagues. The model simulated the process by The pattern of discharge in Rohon-Beard sensory neurons was manipulated which activity in pools of area MT neurons result in a behavioral decision. directly using intracellular stimulation. Depending on the sensory discharge Various parameters and features of the model were adjusted to yield the pattern, either swimming or a struggling-like motor pattern could be elicited: best agreement with the detailed experimental findings. brief discharges caused swimming, whereas repetitive discharges yielded 28. Groh JM, Born RT, Newsome WT: How is a sensory map read the struggling-like pattern. . . out? Effects of microstimulation in visual area MT on saccades 38. Valdez CM, Nishikawa KC: Sensory modulation and behavioral and smooth pursuit eye movements. J Neurosci 1997, 17:4312- choice during feeding in the Australian frog, Cyc/orana 4330. novaehollandiae. J Comp Physiol [Al 1997, 180:187-202. Microstimulation in MT in monkeys making either saccadic and smooth pur- suit eye movements affected both the direction and velocity of the move- 39. Fukai T, Tanaka S: A simple neural network exhibiting selective ments. Usually the microstimulation added a component to the velocity signal activation of ensembles: from winner-take-all to winners- as though the population code used was a vector average rather than other share-all. Neural Comput 1997, 9:77-97. codes, such as vector sum or winner-take-all. These results, along with pre- 40. Shaw BK, Kristan WB: The whole-body shortening reflex vious work [26], suggest that the same area of cortex can be used in more of the medicinal leech: motor pattern, sensory basis, and than one coding scheme, depending upon the task being performed. interneuronal pathways. J Comp Physiol LA] 1995, 177:667- 29. Shadlen MN, Newsome WT: Motion perception: seeing and 681. deciding. Proc Nat/ Acad Sci USA 1996 93:628-633. 41. Ort CA, Kristan WB, Stent GS: Neuronal control of swimming iingle cells were recorded in the lateral intrap&ietal region (LIP), which in the leech. II. Identification and connections of the motor receives input from area MT, using a forced-choice visual discrimination task neurons. J Comp Physiol 1974, 94:121-l 54. similar to that used by the same investigators in studying MT. The activity patterns of some of the LIP neurons indicate that they could be used in 42. Weeks J: Segmental specialization of a leech swim-initiating forming decisions. interneuron, cell 205. J Neurosci 1982, 2:972-985.