Responses of cells in the tail of the caudate nucleus during visual discrimination learning

1. The tail of the caudate nucleus and adjacent ventral putamen (ventrocaudal neostriatum) are major projection sites of the extrastriate visual cortex. Visual information is then relayed, directly or indirectly, to a variety of structures with motor function. To test for a role of the ventrocaudal neostriatum in stimulus-response association learning, or habit formation, neuronal responses were recorded while monkeys performed a visual discrimination task. Additional data were collected from cells in cortical area TF, which serve as a comparison and control for the caudate data. 2. Two monkeys were trained to perform an asymmetrically reinforced go-no go visual discrimination. The stimuli were complex colored patterns, randomly assigned to be either positive or negative. The monkey was rewarded with juice for releasing a bar when a positive stimulus was presented, whereas a negative stimulus signaled that no reward was available and that the monkey should withhold its response. Neuronal responses were recorded both while the monkey performed the task with previously learned stimuli and while it learned the task with new stimuli. In some cases, responses were recorded during reversal learning. 3. There was no evidence that cells in the ventrocaudal neostriatum were influenced by the reward contingencies of the task. Cells did not fire preferentially to the onset of either positive or negative stimuli; neither did cells fire in response to the reward itself or in association with the motor response of the monkey. Only visual responses were apparent. 4. The visual properties of cells in these structures resembled those of cells in some of the cortical areas projecting to them. Most cells responded selectively to different visual stimuli. The degree of stimulus selectivity was assessed with discriminant analysis and was found to be quantitatively similar to that of inferior temporal cells tested with similar stimuli. Likewise, like inferior temporal cells, many cells in the ventrocaudal neostriatum had large, bilateral receptive fields. Some cells had 'doughnut'- shaped receptive fields, with stronger responses in the periphery of both visual fields than at the fovea, similar to the fields of some cells in the superior temporal polysensory area. Although the absence of task-specific responses argues that ventrocaudal neostriatal cells are not themselves the mediators of visual learning in the task employed, their cortical-like visual properties suggest that they might relay visual information important for visuomotor plasticity in other structures. 5. Although there was no evidence of neuronal responses related specifically to the learning of stimulus- response associations in the task, there was a tendency for novel stimuli to elicit stronger neuronal responses than familiar ones. This demonstrates that some form of learning is reflected in the neuronal responses of these neostriatal cells. 6. Cells recorded in cortical area TF were also visually responsive, and many responded selectively to different visual stimuli. In contrast to the ventrocaudal neostriatum, however, responses of a subpopulation of cells in area TF did appear to be influenced by the reward contingencies of the task. That is, some cells responded either preferentially, or even exclusively, to the positive stimuli in the task, a preference that developed within a few trials as the animal learned to discriminate new pairs. These neuronal responses to positive stimuli were not directly related to the motor response of the animal, because they were not present on error trials when the animal responded to the negative stimulus; nor were they directly related to the delivery of the reward, because they were time locked to the onset of the visual stimulus rather than to the reward. The results suggest that some of the mechanisms underlying the learning of stimulus-response associations may be located in the cortex itself.