The middle temporal (MT) and medial superior temporal (MST) areas of the macaque cortex have many cells that respond to straight movements in the frontoparallel plane with directional selectivity (D cells). We examined their responses to movements of a bar, of a wide dot pattern, and to combined movements of the two in anesthetized and immobilized animals. D cells in MT showed a wide variety in the strength of the inhibitory field surrounding the excitatory center field. Responses of SI+-type cells to a bar moving across the excitatory field were suppressed when a wide dot pattern moved over the surround field in the same direction and at the same speed as the bar. Inhibition was selective to the direction and speed of the surround movement, and the effective area for inhibition occupied a wide area, which expanded in all radial directions. Responses of SI- -type cells to a center bar movement were changed little by a conjoint movement over the surround field. Consequently, SI- -type cells responded to wide-field movement as well as to stimuli confined within the excitatory field. Although D cells in MST commonly had large excitatory fields, a proportion of them (Figure type) responded to bar movement much more strongly than to wide-field movement. Their responses to a bar movement were suppressed direction-selectively by a conjoint movement of a wide dot-pattern background. The effective area for inhibition coexisted with the excitatory field in these cells. MST cells of the Nonselective type responded comparably well to the two stimuli, and those of the Field type responded much more strongly to wide-field movement than to bar movement. It is thus suggested that MT cells of the SI+ type and MST cells of the Figure type can detect a difference between movements of an object and its wide background, whereas MST cells of the Field type can detect a conjoint movement of a wide field, neglecting the movements of a single object.

Using anesthetized and paralyzed monkeys, we have studied the visual response properties of neurons in the cortical area surrounding the middle temporal area (MT) in the superior temporal sulcus (STS). Systematic electrode penetrations revealed that there is a functionally distinct region where three classes of directionally selective cells with large receptive fields cluster. This region is anteriorly adjoined to the dorsal two-thirds of MT, has a width of 4-5 mm mediolaterally, and therefore may correspond to the dorsal part of the medial superior temporal area (MST), which was previously defined as a MT-recipient zone. One class of cells responded to a straight movement of patterns in the frontoparallel plane with directional selectivity (D cells: 217/422, 51.4%). The second class of cells selectively responded to an expanding or contracting size change of patterns (S cells: 66/422, 15.7%). These cells responded neither to a change in width of a slit of any orientation or any length, nor to a change in brightness. The third class of cells responded only to a rotation of patterns in one direction (R cells: 58/422, 13.7%). A majority of these cells (41/58) responded to the clockwise or counterclockwise rotation of patterns in the frontoparallel plane (Rf cells), while the rest responded to a rotation of patterns in depth (Rd cells). We will suggest that these cells acquire the ability to discover whole events of visual motion--i.e., unidirectional straight movement, size change (radial movement), and rotation--by integrating elemental motion information extracted by MT cells. The receptive fields of D, S, and Rf cells can be constructed by converging signals of MT cells, the preferred directions of which are arranged in parallel (D cells), radially (S cells), and circularly (Rf cells). The receptive fields of Rd cells can be constructed, in turn, by the convergence of signals of S cells.

We examined neuronal activity in the orbitofrontal cortex (OFC) in relation to reward expectancy and compared findings with those of the lateral prefrontal cortex (LPFC) in the monkey. Activity of OFC neurons was examined in a delayed reaction time task where every four trials constituted one block within which three kinds of rewards and no reward were delivered in a fixed order. More than half of OFC delay neurons were related to the expectancy of delivery or nodelivery of a reward as the response outcome, while some neurons showed nature-of-reward-specific anticipatory activity changes. These delay-related activities reflected the preference of the animal for each kind of reward and were modulated by the motivational state of the animal. LPFC neurons are reported to show nature-ofreward-specific anticipatory activity changes in a delayed response task when several different kinds of rewards are used. Such rewarddependent activity is observed in LPFC delay neurons both with and without spatially differential delay (working memory-related) activity. Although reward expectancy-related activity is commonly observed in both OFC and LPFC, it is suggested that the OFC is more concerned with motivational aspects, while the LPFC is related to both the cognitive and motivational aspects of the expectancy of response outcome.

1. We examined the sensory properties of cells in the anterior bank of the caudal part of the superior temporal sulcus (caudal STS) in anesthetized, paralyzed monkeys to visual, auditory, and somesthetic stimuli. 2. In the anterior bank of the caudal STS, there were three regions distinguishable from each other and also from the middle temporal area (MT) in the floor of the STS and area Tpt in the superior temporal gyrus. The three regions were located approximately in the respective inner, middle, and outer thirds of the anterior bank of the caudal STS. These three regions are referred to, from the inner to the outer, as the medial superior temporal region (MST), the mostly unresponsive region, and the caudal STS polysensory region (cSTP), respectively. 3. The extent of MST and its response properties agreed with previous studies. Cells in MST responded exclusively to visual stimuli, had large visual receptive fields (RFs), and nearly all (91%) showed directional selectivity. 4. In the mostly unresponsive region, three quarters of cells were unresponsive to any stimulus used in this study. A quarter of the cells responded to only visual stimuli and most did not show directional selectivity for moving stimuli. Several directionally selective cells responded to movements of three-dimensional objects, but not of projected stimuli. 5. The response properties of cells in the superficial cortex of the caudal superior temporal gyrus, a part of area Tpt, external to cSTP were different from those of cells in the three regions in the anterior bank of the STS. Cells in Tpt were exclusively auditory, and had much larger auditory RFs (mean = 271 degrees) than those of acoustically-driven cSTP cells (mean = 138 degrees). 6. The cSTP contained unimodal visual, auditory, and somesthetic cells as well as multimodal cells of two or all three modalities. The sensory properties of cSTP cells were as follows. 1) Out of 200 cells recorded, 102 (51%) cells were unimodal (59 visual, 33 auditory, and 10 somesthetic), 36 (18%) cells were bimodal (21 visual+auditory, 7 visual+somesthetic, and 8 auditory+somesthetic), and four (2%) cells were trimodal. Visual and auditory responses were more frequent than somesthetic responses: the ratio of the population of cells driven by visual: auditory: somesthetic stimuli was 3:2:1. 2) Visual RFs were large (mean diameter, 59 degrees), but two-thirds were limited to the contralateral visual hemifield. About half the cells showed directional selectivity for moving visual stimuli. None showed selectivity for particular visual shapes.(ABSTRACT TRUNCATED AT 400 WORDS)

Increase of extracellular dopamine in primate prefrontal cortex during a working memory task. J. Neurophysiol. 78: 2795-2798, 1997. The dopamine innervation of the prefrontal cortex is involved importantly in cognitive processes, such as tested in working memory tasks. However, there have been no studies directly investigating prefrontal dopamine levels in relation to cognitive processes. We measured frontal extracellular dopamine concentration using in vivo microdialysis in monkeys performing in a delayed alternation task as a typical working memory paradigm and in a sensory-guided control task. We observed a significant increase in dopamine level in the delayed alternation task as compared both with the sensory-guided control task and the basal resting level. The increase was seen in the dorsolateral prefrontal but not in the arcuate or orbitofrontal areas. The increase appeared to reflect the working memory component of the task and was observed mainly in the lip areas of principal sulcus. Although there was no significant difference in dopamine level between delayed alternation and sensory-guided control tasks in the premotor area, significant increases in dopamine concentration were observed during both tasks as compared with the basal resting level, indicating the importance of premotor dopamine for the motor response itself.

The prefrontal cortex is involved in acquiring and maintaining information about context, including the set of task instructions and/or the outcome of previous stimulus-response sequences. Most studies on context-dependent processing in the prefrontal cortex have been concerned with such executive functions, but the prefrontal cortex is also involved in motivational operations. We thus wished to determine whether primate prefrontal neurons show evidence of representing the motivational context learned by the monkey. We trained monkeys in a delayed reaction task in which an instruction cue indicated the presence or absence of reward. In random alternation with no reward, the same one of several different kinds of food and liquid rewards was delivered repeatedly in a block of approximately 50 trials, so that reward information would define the motivational context. In response to an instruction cue indicating absence of reward, we found that neurons in the lateral prefrontal cortex not only predicted the absence of reward but also represented more specifically which kind of reward would be omitted in a given trial. These neurons seem to code contextual information concerning which kind of reward may be delivered in following trials. We also found prefrontal neurons that showed tonic baseline activity that may be related to monitoring such motivational context. The different types of neurons were distributed differently along the dorsoventral extent of the lateral prefrontal cortex. Such operations in the prefrontal cortex may be important for the monkey to maximize reward or to modify behavioral strategies and thus may contribute to executive control.

Learning theory emphasizes the importance of expectations in the control of instrumental action. This study investigated the variation of behavioral reactions toward different rewards as an expression of differential expectations of outcomes in primates. We employed several versions of two basic behavioral paradigms, the spatial delayed response task and the delayed reaction task. These tasks are commonly used in neurobiological studies of working memory, movement preparation, and event expectation involving the frontal cortex and basal ganglia. An initial visual instruction stimulus indicated to the animal which one of several food or liquid rewards would be delivered after each correct behavioral response, or whether or not a reward could be obtained. We measured the reaction times of the operantly conditioned arm movement necessary for obtaining the reward, and the durations of anticipatory licking prior to liquid reward delivery as a Pavlovian conditioned response. The results showed that both measures varied depending on the reward predicted by the initial instruction. Arm movements were performed with significantly shorter reaction times for foods or liquids that were more preferred by the animal than for less preferred ones. Still larger differences were observed between rewarded and unrewarded trials. An interesting effect was found in unrewarded trials, in which reaction times were significantly shorter when a highly preferred reward was delivered in the alternative rewarded trials of the same trial block as compared to a less preferred reward. Anticipatory licks preceding the reward were significantly longer when highly preferred rather than less preferred rewards, or no rewards, were predicted. These results demonstrate that behavioral reactions preceding rewards may vary depending on the predicted future reward and suggest that monkeys differentially expect particular outcomes in the presently investigated tasks.

Two-photon imaging in behaving animals has revealed neuronal activities related to behavioral and cognitive function at single-cell resolution. However, marmosets have posed a challenge due to limited success in training on motor tasks. Here we report the development of protocols to train head-fixed common marmosets to perform upper-limb movement tasks and simultaneously perform two-photon imaging. After 2–5 months of training sessions, head-fixed marmosets can control a manipulandum to move a cursor to a target on a screen. We conduct two-photon calcium imaging of layer 2/3 neurons in the motor cortex during this motor task performance, and detect task-relevant activity from multiple neurons at cellular and subcellular resolutions. In a two-target reaching task, some neurons show direction-selective activity over the training days. In a short-term force-field adaptation task, some neurons change their activity when the force field is on. Two-photon calcium imaging in behaving marmosets may become a fundamental technique for determining the spatial organization of the cortical dynamics underlying action and cognition.