Movement and non-movement related pallidal unit activity during bar press feeding behavior in the monkey

Activity was recorded from 358 neurons in the globus pallidus (GP) of monkeys (Macaca fuscata) during an operant feeding task consisting of 3 stages: (1) food or non-food presentation (1st stage); (2) bar pressing (2nd stage); and (3) food acquisition and ingestion (3rd stage). There were two kinds of neurons, one with high and the other with very low (almost silent), spontaneous firing rates. Two hundred and four neurons (57%) responded in one or more of the feeding stages. Of the 21 neurons which responded in the 1st stage, two responded selectively to food presentation, and 19 responded to both food and non-food visual presentation. One hundred and seventy-four neurons (49%) and 107 neurons (30%) responded in the 2nd and 3rd stages, respectively, and 106 (30%) of these were directly related to specific feeding motor acts such as arm extension, flexion, bar pressing, grasping, chewing etc. Both high and low firing neurons responded to motor acts with sharp or gradual onset. More than half of those that responded to arm extension showed laterality (contra or ipsi)- and function (extension or flexion)-dependent responses. The incidence of the motor related neurons was higher in the caudodorsal part of the GP. On the other hand, about one third, especially in the rostroventral part of the GP, showed dissociating responses in that they responded during bar pressing for food or during ingestion in an operant task, but not during bar pressing for non-food or during forcible ingestion. The magnitude of firing changes during arm extension and bar pressing depended on the nature of the food. Moreover, in trials using new food or false (model) food, firing changes during bar press appeared or disappeared within a few trials with no correlation to bar press movement. These data suggest heterogeneous functions within the GP; the caudodorsal part is strictly concerned with motor execution and preparation, while the rostroventral part is not related to motor function directly, but may rather be important in coupling internal, motivational information to the motor system.     

Functional role of the limbic system and basal ganglia in motivated behaviors

It has been suggested that the cortico- and limbic-striatal systems are important in various motor functions such as motivated behaviors. In this paper we review our previous studies to investigate neuronal mechanisms of feeding behaviors. We recorded neuronal activity from the amygdala, caudate nucleus, globus pallidus, and substantia nigra during feeding behavior in monkeys, and compared neuronal responses recorded from these brain areas. First, of 710 amygdalar neurons tested, 129 (18.2%) responded to single sensory stimulation (48 to vision, 32 to audition, 49 to ingestion), 142 (20%) to multimodal stimulation, and 20 to only one item with affective significance. Eight food related amygdalar neurons were tested in reversal by salting food or introducing saline, and all responses were modulated by reversal. These results suggest that the amygdala might be important in ongoing recognition of the affective significance of complex stimuli (food-nonfood discrimination).

Second, activity was recorded from 351 neurons in the head of the caudate nucleus of monkeys during an operant feeding task. The 16% of these neurons responded in the discrimination phase. Some of these neurons responded specifically to food. The magnitude of these food-specific neurons depend on the rewarding nature of the food (reward value), and was inversely related to the latency of the onset of bar press. Of the caudate neurons, 10% responded in the bar press phase. Activity of most neurons which responded in the bar press phase was not correlated to individual bar presses. Cooling of the dorsolateral prefrontal cortex abolished sustained responses during bar pressing, but did not abolish the feeding behavior. However, bar press speed tended to be delayed by prefrontal cooling.

Third, activity of 358 neurons was recorded from the monkey globus pallidus, and 204 neurons responded during the feeding task. In the globus pallidus, few neurons responded to food in the discrimination phase. On the other hand, activity of most responsive neurons changed during bar press and/or ingestion phases. Activity of about half of these responsive neurons was directly related to specific feeding motor acts such as arm extension, flexion, bar pressing, grasping, chewing, etc. Some of these neurons showed motor-related responses with gradual and preparatory responses. These motor-related neurons were located mainly in the caudodorsal part of the globus pallidus. On the other hand, about one third, especially in the rostroventral part of the globus pallidus, showed dissociating responses in that they responded during bar pressing for food or during ingestion in an operant task, but not during bar pressing for nonfood or during forcible ingestion. The response magnitude of the neurons during arm extension and bar pressing depended on the nature of the food.

Fourth, activity of 261 neurons was recorded from the substantia nigra pars reticulata. Most of responding neurons (more than two-thirds of the recorded neurons) responded during the bar press and/or ingestion phases. Activity of the one-third of neurons was related to specific motor execution such as arm extension, flexion and bar pressing, but not to motor preparation. These neurons were located mainly in the rostral part of the nucleus. More than one-third of the recorded neurons responded during feed and/or drinking acts and intra- and perioral sensory stimuli, and were located mainly in the caudomedial part of the nucleus.

Based upon these responses and known anatomical evidence, various information including that from the amygdala and prefrontal cortex is integrated in the basal ganglia, and converted to coordinated motivated behaviors such as feeding behavior.

     

Single neuron activity in dorsolateral prefrontal cortex of monkey during operant behavior sustained by food reward

The activity of 190 neurons was recorded from the dorsolateral prefrontal cortex of monkeys during an operant task that consisted of 3 phases: visual discrimination of food and non-food, bar pressing to gain access to the food and ingestion. In area 8, a fairly large proportion of the 49 recorded neurons responded in both the visual discrimination (37%) and motor initiation (35%) phases. Some functional heterogeneity seems evident within area 8 since visual discrimination responses were rostral, visuokinesis was central and motor initiation was in the caudal bank of the arcuate sulcus. Neurons in area 9 responded primarily (37%) during the bar pressing phase and less during the visual discrimination phase. Neurons in area 10 responded variously during most phases of the task--food discrimination, bar pressing, and ingestion. Neurons in the periprincipal sulcal area usually responded in the visual discrimination phase, but some which did not respond to food presented in front of the subject responded to meaningful visual or auditory cues that were related to food reward. The data suggest that neurons in the dorsolateral prefrontal cortex have multiple functions related to all phases of complex, learned feeding behavior. Functional roles of the prefrontal cortex and the lateral hypothalamus in development of feeding behavior are discussed.     

Visual responses related to food discrimination in monkey lateral hypothalamus during operant feeding behavior

Single neuron activity was recorded from monkey lateral hypothalamic area (LHA) to relate neuronal events to food discrimination and initiation of procurement movement in operant bar press feeding behavior. Of 429 neurons tested, 68 (16%) responded during visual phase. Of these, 30 (7%) responded selectively to the sight of food or non-food associated with a juice reward, but not to the sight of meaningless non-food or food associated with aversive saline. Neuronal activity related to discrimination was readily influenced by extinction, reversal or satiation. The strength of visual responses was correlated with latency of bar press initiation and speed of bar pressing, but was not related directly to bar press movement. These suggest that the LHA is deeply involved in discrimination of reinforcement or non-reinforcement, and might be associated with higher functions to regulate internal states such as physiological need to get food during operant feeding behavior.     

Basal ganglia neural activity during operant feeding behavior in the monkey: relation to sensory integration and motor execution

The activity of single neurons in the caudate nucleus (CD), globus pallidus (GP), substantia nigra pars reticulata (SNr), and ventral tegmental area (VTA) was recorded during an operant feeding task in the monkey. The task had three phases: recognition of the food or nonfood stimulus (1st phase), bar pressing to obtain access to the stimulus (2nd phase), and ingestion (3rd phase). Data were collected from 351 neurons in CD, 344 in GP, 261 in SNr, and 275 in VTA. Neurons in the dorsolateral part of the CD, GP, and SNr responded primarily to motor events of feeding, i.e., extension/flexion of the arm, bar pressing, chewing, grasping or gazing. Neurons in the ventromedial part of the CD and rostroventral part of the GP exhibited differential responses to the presentation of food and nonfood during the recognition and bar pressing phases of the task. Neurons in the VTA increased their firing early in the bar pressing phase and then decreased their firing during ingestion. The data suggest that the dorsolateral part of the basal ganglia is involved mainly in motor function, while the ventromedial part may reflect the connection between motivation and motor output.     

Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance

Among other deficits, amygdalectomy impairs the ability of the animal to recognize the affective significance of a stimulus. In the present study, neuronal activity in the amygdala (AM) was recorded from alert monkeys while they performed tasks leading to the presentation of rewarding or aversive stimuli. Of 585 AM neurons tested, 312 (53.3%) responded to at least one stimulus in one or more of 5 major groups: 40 vision related, 26 audition related, 41 ingestion related, 117 multimodal, and 14 selective. Ingestion-related neurons were subdivided according to their responses to other stimuli: oral sensory, oral sensory plus vision, and oral sensory plus audition. Depending upon their responsiveness to the affective significance of the stimuli, neurons in the vision- and audition-related categories were divided into 2 subclasses: vis-I (26/40), vis-II (14/40), aud-I (8/26), and aud-II (18/26). All 4 subtypes usually responded to unfamiliar stimuli but seldom responded to neutral familiar stimuli. Types vis-I and aud-I responded to both positive and negative familiar stimuli. Types vis-II and aud-II responded to certain familiar negative stimuli but not to familiar positive stimuli. In vis-I neurons, responses were stronger for palatable foods than for less palatable foods. No neurons within vision-related, audition-related, and multimodal categories responded solely to positive or to negative stimuli. Of the 27 oral sensory neurons 9 were tested with saline or salted food, and 8 responded to normally aversive oral sensory stimuli in the same manner as they did to normal food or liquid (water or juice). In contrast to oral sensory neurons, all responses of 4 oral sensory-plus-vision and all of 4 selective neurons tested, as well as bar pressing behavior, were modulated by altering the affective significance of the food. These results suggest that the AM is one of the candidates for stimulus-affective association based on associative learning and memory.     

Amygdaloid neuronal responses to complex visual stimuli in an operant feeding situation in the monkey

In chronically prepared monkeys, 337 neurons were recorded from the anterolateral amygdala during an operant task that required visual discrimination. Twelve percent (39/337) of the neurons responded to one or more of food or non-food visual stimuli. A subset of these responsive neurons was selectively sensitive to the sight of non-food objects with aversive associations. Simultaneous presentation of a food stimulus with the aversive object inhibited the response of these neurons. These response characteristics could not be explained by simple sensory processing of the visual stimuli. It is suggested that the amygdala plays an important role in the elaboration of motivational behavior by using the complex or associative properties of visual stimuli.     

Neuronal responses in monkey anterior putamen during operant bar-press behavior

Single neuron activity was recorded in the monkey anterior putamen to compare visuomotor-related responses during operant bar-press behavior with visual discrimination of objects. Of 615 neurons recorded 9.8% ( ) responded to the presentation of food during forced delay of access to the bar. Of these 60 neurons, 38 were also tested with nonfood, and 19 of these responded to the nonfood objects regardless of the following movement. The amplitude of the visual-related responses of some differential neurons was graded for different objects to reflect the relative degree of preference for the food presented. However, these responses disappeared in reaction time tasks in which the bar could be accessed for pressing immediately upon presentation of an object. The visual response latency of differential neurons ranged from 50 to 700 ms (mean ± SD, 386 ±211 ms), which was longer than that of the nondifferential responses (207 ± 204 ms). These results suggest that anterior putamen neurons might participate in estimation of visual information that could be related to forecasting movement.     

Neuronal responses in monkey lateral hypothalamus during operant feeding behavior

Single neuron activity was recorded from monkey lateral hypothalamus to investigate neuronal events correlated with operant bar press feeding behavior. The behavioral paradigm was divided into three phase: visual (discrimination), bar press (procurement), and ingestion (consummatory). Of 669 neurons tested, 158 (24%) responded in one or more phases. During the visual phase, 106 neurons (16%) responded. Of 80 neurons that responded in the visual phase and were tested systematically, 33 (41%, 33/80) responded selectively to the sight of food or nonfood objects associated with a juice reward, but not to the sight of nonfood or objects associated with aversive saline. Neuronal activity related to discrimination was modulated by satiation and learning (i.e., acquisition and extinction). During the bar press phase, 51 neurons (7.6%) responded. These responded tonically during the early or late stage of the bar press period, but did not depend on individual bar pressing motions. During ingestion, 90 neurons (13%) responded. The ingestion response was modulated by palatability of food and satiation. Data suggest that the LHA is deeply involved in operant feeding behavior; discrimination of food, drive to get food, and perception of reward, all of which are affected by learning and internal states such as hunger and satiety.     

Neuronal activity in the ventral tegmental area (VTA) during motivated bar press feeding in the monkey

Neuronal activity of 58 dopaminergic (DA) and 200 non-dopaminergic (non-DA) neurons in the ventral tegmental area (VTA) of female monkeys was recorded, and correlation to bar press feeding, sensory stimulation and change in motivation was investigated. DA neurons, judged by duration of action potentials (more than 2.5 ms) and responsiveness to apomorphine, had lower firing rates (0-8 impulses/s); non-DA neurons had intermediate firing rates (10-30 impulses/s). Two-thirds of the DA and non-DA neurons responded in bar press feeding; the former with mostly tonic and the latter with phasic responses. Fifteen neurons (5%) responded phasically to arm extension toward the bar, 124 (excitation 88, inhibition 36, 45%) during bar press (BP), and 91 (excitation 32, inhibition 59, 33%) during ingestion reward (RW). Most BP responses (84/124, 68%) continued tonically throughout the BP period with no correlation to each BP movement. In 14 neurons (14/124, 11%), firing showed a specific variation: transient early BP responses shifted to tonic steady ones in palatable food trials, and the shifts correlated well with BP speed. In 20 other neurons, firing increased during BP hip lifting, and at specific vocalization to ask for food; it decreased during food ingestion, drinking and inguino-crural stimulation. Apomorphine administration decreased firing for the first 5-15 min, then increased it with frequent lip smacking, nausea, involuntary movement and vocalization. Thus VTA neurons showed mostly steady tonic responses but some specific phasic responses. They responded not only to motor events but also in close relation to changes of motivational aspects. Neuronal responses were excitation during procurement of reward and inhibition during or after perception of reward. This modulation in firing, might be important in the initiation and execution of movement and/or motivated behavior.     

Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus

The activity of 394 neurons in the head of the caudate nucleus and the most anterior part of the putamen was analyzed in 3 behaving rhesus monkeys in order to analyze the functions of this part of the striatum. Of these neurons, 64.2% responded in the tests used in relation to, for example, environmental events, movements made by the monkey, the performance of a visual discrimination, or during feeding. However, only relatively small proportions of these neurons had responses which were unconditionally related to visual (9.6%), auditory (3.5%), or gustatory (0.5%) stimuli, or to movements (4.1%). Instead, the majority of the responsive neurons had activity in relation to stimuli or movements which was conditional, in that the responses occurred in only some test situations, and were often dependent on the performance of a task by the monkeys. Thus, it was found in the visual discrimination task that 14.5% of the neurons responded during a 0.5 sec tone/light cue period which signalled the start of each trial; 31.1% responded in the period in which the discriminative visual stimuli were shown, with 24.3% of these responding more to either the visual stimulus which signified food reward or to that which signified punishment; and 6.2% responded in relation to lick responses. Yet these neurons typically did not respond in relation to the cue stimuli, to the visual stimuli, or to movements, when these occurred independently of the task, or when performance of the task was prevented. Comparably, of the neurons tested during feeding, 25.8% responded when the food was seen by the monkey, 6.2% when he tasted it, and 22.4% during a cue given by the experimenter that a food or non-food object was about to be presented. However, only few of these neurons had responses to the same stimuli presented in different situations.It is concluded that many neurons in the head of the caudate nucleus and the most anterior part of the putamen respond in relation to events which are used as cues to prepare for the performance of tasks, including feeding, in which movements must be initiated. Other neurons respond in relation to the stimuli used and the movements made in these tasks. However, the majority of these neurons do not have unconditional sensory or motor responses. It is therefore suggested that the anterior neostriatum contains neuronal mechanisms which are important in the process by which environmental cues are used in the preparation of behavioral responses, and in the initiation of particular behavioral responses made in particular situations to particular environmental stimuli. Deficits in the initiation of movements following damage to striatal pathways may arise in part because of interference with these functions of the anterior neostriatum.     

Topographic distribution of modality-specific amygdalar neurons in alert monkey

Neuronal activity in the amygdala (AM) was recorded from alert monkeys during performance of tasks that led to presentation of rewarding or aversive stimuli. The tasks had 3 phases: (1) discrimination (visual, auditory), (2) operant response (bar pressing), and (3) ingestion (reward) or avoidance (aversion). Neuronal activity was analyzed and compared during each of these phases. Of 585 AM neurons tested, 312 (53.3%) responded to at least one stimulus in one or more of 5 major groups: vision related, audition related, ingestion related, multimodal, and selective. Forty neurons (6.8%) in the anterior dorsolateral capsule of the basolateral nuclei responded exclusively to visual stimuli (vision related). Twenty-six neurons (4.4%) further posterior in the basolateral group responded only to auditory stimuli (audition related). During ingestion an additional 41 neurons (7.0%) increased their activity (ingestion related). These were in the corticomedial group and at the boundaries between the nuclei of the basolateral group. Of these, 27 responded only in the ingestion phase, 11 during ingestion and at the sight of food, and 3 during ingestion and to certain sounds. Throughout the AM other neurons (n = 117, 20.0%) responded to visual, auditory, and somesthetic stimuli and, when tested, to involuntary ingestion of liquid (multimodal). Of these, 40 responded transiently (phasic; 36 excited, 4 inhibited). The remaining 77 maintained their altered activity into the subsequent phases of the task (tonic; 69 excited, 8 inhibited). In each of these 4 categories, most cells were activated primarily by novel or unfamiliar stimuli, and their responses habituated during repeated stimulation. A small number of cells in the basolateral and the basomedial nuclei (n = 14, 2.4%) were highly selective in that they responded specifically to one biologically significant object or sound more than to any other stimuli (selective). Some of these neurons responded to both sight and ingestion of a specific food. In summary, most AM neurons responded vigorously to novel stimuli, and some of the neurons had multimodal responsiveness. These results suggest the AM is related to processing of new environmental stimuli and to those cross-modal association.     

Behavioral significance of monkey hypothalamic glucose-sensitive neurons

Feeding-related neuronal activity of lateral hypothalamic glucose-sensitive and glucose-insensitive neurons was investigated in behaving monkeys. The behavioral paradigm was a high fixed ratio of bar pressing for food reward signaled by light and tone cues. Twenty-seven percent of the neurons tested were glucose-sensitive. The population of neurons which changed in firing rate during the feeding task was higher among glucose-sensitive cells than among glucose-insensitive cells. The activity of many glucose-sensitive neurons decreased during the bar pressing and reward periods. A small population of glucose-sensitive neurons responded to cue stimuli. The results suggest that glucose-sensitive neurons are mainly involved in the drive and/or reward mechanism of feeding behavior, and that these cells may have specific roles in neural control of hunger-motivated food acquisition.     

Catecholaminergic mechanisms of feeding-related lateral hypothalamic activity in the monkey

The functional role of the catecholaminergic mechanism in the lateral hypothalamus (LHA), in feeding behavior of the monkey was investigated by single neuron activity recording and electrophoretic application of dopamine (DA), noradrenaline (NA) and their antagonists. The feeding paradigm had 4 phases: cue light (CL) signaled start of bar press; bar press (BP, 20-30 times); short cue tone (CT) triggered by last bar press signaled presentation of food; and ingestion-reward (RW). Of 312 neurons tested, 189 (61%) responded in one or more phases of the feeding task. Two types of response were observed: CL- or CT-related transient, and BP- or RW-related long-lasting responses. These feeding-related responses depended on the nature of the food and on the hunger-satiety level. DA excited or inhibited different neurons, while NA mainly inhibited firing. DA-sensitive neurons responded more often in the feeding task than insensitive neurons due mainly to differences in responsiveness to CL on (chi 2 test, P less than 0.01), at motor initiation, and during BP (P less than 0.05). Spiperone blocked the former two responses. NA-sensitive neurons responded more often in the feeding task due to responsiveness during BP and RW (P less than 0.01). Sotalol blocked some BP-related responses, and phenoxybenzamine and sotalol blocked the CT-related responses. The data suggest that dopaminergic and noradrenergic inputs in the LHA are crucial in task initiation and reward processing, respectively. Integration of these catecholaminergic and other inputs in the LHA might be important in accomplishing motivated feeding.     

Interneurons in the tritocerebrum of the crayfish

In isolated head preparations of the freshwater crayfish Orconectes limosus 268 local and projecting interneurons with branches in the tritocerebrum have been penetrated with glass microelectrodes and characterized for their sensory inputs. Using 3 criteria (sensory modality, site of receptors, response type of interneurons), the interneurons found were divided into 16 classes. The interneurons were either unimodal mechanoreceptive (89%) or bimodal (9% responding to mechanical and chemical stimuli, 2% responding to mechanical and visual stimuli). No trimodal interneurons were found. Within each modality the neurons received mostly bilateral input (70% of all interneurons responding to antennal stimulation, 84% of all chemosensitive interneurons). If the input was lateralized it was more often ipsilateral. The types of interneuronal responses evoked by sensory stimulation were: neurons that were exclusively excited (84%), those that were exclusively inhibited (10%), those that were excited or inhibited depending on the modality or laterality of the stimulus (6%), those showing long lasting excitatory aftereffects (3%), and those showing excitation or inhibition upon identical stimulation depending on the state of the neurons while being stimulated (1%). Interneurons that responded to mechanical antennal stimulation responded best either to low (10 Hz) or to high (100 Hz) stimulus frequencies. Six neurons responded best to a certain phase relationship between the movements of both antennal flagellae.     

Single unit response types in the pulvinar of the Cebus monkey to multisensory stimulation

Response to sensory stimulation was studied in 162 neurons in the pulvinar of Cebus monkeys in 4 acute and 5 chronic preparations. Two basic response patterns were observed: type I responses, similar to those obtained in primary relay centers, were only observed after visual stimulation. Type II responses were obtained after stimulation of more than one sensory modality. Characteristically these responses presented fatigue and habituation. Temporal relationship between stimulus and response was not as clear as in type I responses, afterdischarge frequently occurred. Taking these response types into consideration two groups of units were identified in the pulvinar. Units of group A (91 neurons) showed type I response to visual stimulation. For these units receptive fields similar to those found in other regions of visual projection could be defined. As a rule units of group A displayed type II responses to other sensory modalities. Units of group B (71) did not display type I responses; they always responded to visual, somatic, auditory and olfactory stimuli with type II responses. They could be activated by a single sensory modality (B, unimodal) or by more than one sensory modality (B, multimodal).     

Neural correlates to both emotion and cognitive functions in the monkey amygdala

Recent lesion and non-invasive studies identify the medial temporal lobe, including the amygdala, not only with emotion but also with working memory in relation to the prefrontal cortex. In the present study, amygdalar neuronal activity was recorded from monkeys during performance of discrimination tasks that led to presentation of emotion-related (rewarding or aversive) stimuli. The task had three phases: (1) discrimination (visual, auditory), (2) operant response (bar pressing) and (3) ingestion (reward) or avoidance (aversion). These neurons were further analyzed by a short-term memory task, delayed pair comparison (DPC) using colored lamps. Of 585 amygdalar neurons, 107 responded primarily to single sensory stimulation (40 vision related, 26 audition related, 41 ingestion related), 117 to multimodal stimulation (multimodal) and 14 responded selectively to only one item (selective). Of 417 neurons tested by the DPC, 122 responded in one or more phases. Of these 122 neurons, 10.7% responded in the delay period. These delay-responsive neurons also responded to various objects with positive and negative affective significance. These results suggest that amygdalar neurons are not specifically related to working memory, as are those in the inferotemporal and prefrontal cortices, but are related to more general non-specific functions or processes such as arousal or attention during the cognitive tasks. A functional role of the amygdala in working memory is discussed in terms of recent non-invasive studies suggesting a functional coupling between the amygdala and prefrontal cortex.     

Neuron activity in and adjacent to the dorsal amygdala of monkey during operant feeding behavior

Neuronal activity of the dorsal amygdala, the substantia innominata and the ventral putamen during bar press operant behavior was analyzed to investigate neuronal responses in various affective situations. Of 1507 neurons recorded, 431 responded to some stimuli and were classified into 6 functional categories: 64 (4.2%) indiscriminately and transiently responded to various stimuli; 98 (6.5%) responded to various objects depending on their significance, whether rewarding or punishing; 44 (2.9%) clearly responded only to certain food or objects associated with potables, but not to both; 16 (1.1%) responded to both food and objects associated with potables; 35 (2.3%) responded primarily at the sight of certain nonfood; 66 (4.4%) responded primarily in the ingestion phase. Relations between function and topography are discussed. The results suggest that the dorsal AM and adjacent areas might be important in recognizing the biological significance of objects and in procuring food.     

Context-dependent responses of primate nucleus basalis neurons in a go/no-go task

In previous studies involving monkeys performing behavioral tasks, neurons in the nucleus basalis frequently had significant changes in discharge rate when the animal made a movement in response to a sensory stimulus in order to obtain a reward. To determine whether such responses of basalis neurons are primarily sensory or motor in nature, the activity of single basalis neurons was recorded in monkeys performing a go/no-go (GNG) task which provided a dissociation between sensory and motor neuronal responses. In a sample of 425 basalis neurons, 326 (77%) had significant changes in firing in at least one phase of the GNG task. Most of the task-related neurons (70%) responded in the choice phase in which the animal either made an arm movement (go condition) or kept its arm motionless (no-go condition) in order to obtain a water reward. Of 253 neurons that responded in the choice phase, 88% had changes in firing in the no-go condition that were equal to or, in some cases, greater than the changes in firing in the go condition. Therefore, most responses of basalis neurons in the choice phase could not be specific for the arm movement because they occurred when there was no arm movement at all. The visual stimulus presented in the choice phase was also presented earlier on each trial in the cue phase. Although 70% of the task-related basalis neurons responded in the choice phase, only 5% had detectable changes in firing in the cue phase. Of 251 neurons responding in the cue or choice phase, 59% had significantly larger changes in firing in the choice phase than in the cue phase, whereas only one neuron had a larger response in the cue phase. Therefore, most responses of basalis neurons in the choice phase could not be specific for the visual stimulus because similar responses did not occur when the same stimulus was presented in the cue phase. These results indicate that the frequent responses of basalis neurons in the choice phase are neither purely sensory nor motor in nature, but are highly dependent on the context of the stimulus or movement. The neuronal responses in the choice phase may reflect either transient increases in arousal or decision-making processes.     

Hippocampal neuronal responses during signaled licking of gustatory stimuli in different contexts

Neuroanatomical studies suggest that hippocampal formation (HF) receives information from all sensory modalities including taste via the parahippocampal cortices. To date, however, no neurophysiological study has reported that HF neurons encode taste information. In the present study, we recorded CA1 HF neurons from freely behaving rats during performance of a visually‐guided licking task in two different triangular chambers. When a cue lamp came on, the rats were required to press a bar to trigger a tube to protrude into the chambers for 3 s. During this period, the rats could lick one of six sapid solutions: [0.1M NaCl (salty), 0.3M sucrose (sweet), 0.01M citric acid (sour), 0.0001M quinine HCl (bitter), 0.01M monosodium L ‐glutamate (MSG, umami), and a mixture of MSG and 0.001M disodium‐5′‐inosinate (IMP) (MSG+IMP)], and distilled water. Of a total 285 pyramidal and interneurons, the activity of 173 was correlated with at least one of the events in the task—illumination of cue lamps, bar pressing, or licking the solution. Of these, 137 neurons responded during licking, and responses of 62 of these cells were greater to sapid solutions than to water (taste neurons). Multivariate analyses of the taste neurons suggested that, in the HF, taste quality might be encoded based on hedonic value. Furthermore, the activity of most taste neurons was chamber‐specific. These results implicate the HF in guiding appetitive behaviors such as conditioned place preference. © 2010 Wiley‐Liss, Inc.