Functional properties of monkey caudate neurons. II. Visual and auditory responses.

1. Visual responses of caudate neurons were studied in monkeys trained to fixate on a small spot of light. A visual stimulus (another spot of light) was presented in various contexts of behavior using different behavioral paradigms. Visual receptive fields were usually large and centered on the contralateral hemifield. Among 217 neurons with visual responses, 184 were further classified into subtypes. 2. Visual responses in 64 neurons were not modulated by changing the paradigms (unconditional visual responses). In the other neurons, visual responses were dependent on the behavioral contexts in which the stimulus was presented. Three types of behavioral modulation were found. 3. A saccade-enhanced visual response (n = 37) was the one that was enhanced if the monkey made a saccade to the stimulus on its appearance. The enhancement was spatially selective: the response was depressed if the saccade was directed away from the stimulus. 4. Memory-contingent visual responses (n = 36) were present preferentially when the monkey remembered the location of the stimulus and a few seconds later made a saccade to the remembered location. Responses were greater when the location of the stimulus was randomized between trials. 5. Expectation-contingent visual responses (n = 46) were present preferentially when the stimulus came on while the monkey was not fixating another spot, and the stimulus was related directly to a reward. Unlike the other types, its receptive field included both contralateral and ipsilateral hemifields without a particular preference. 6. A small number of neurons (n = 16) showed a visual response that easily habituated. 7. Latencies of visual responses were usually between 100 and 200 ms. The latencies of the memory-contingent, expectation-contingent, and habituated visual responses tended to be longer than the others and tended to be more variable between trials. 8. Among auditory responsive neurons only a small proportion were related to the tasks. The response was greater to a contralateral sound. It was enhanced if the monkey used the sound as the cue for the future target location. 9. The results suggest that sensory responses of caudate neurons could be used to guide a subsequent sequence of learned behaviors by confirming predicted environmental states, renewing memory, or establishing a motor set.

[1]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. II. Visual responses related to fixation of gaze. , 1983, Journal of neurophysiology.

[2]  W. Schultz Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory, and complex events. , 1986, Journal of neurophysiology.

[3]  R. Wurtz,et al.  Behavioral correlates of activity in basal ganglia neurons , 1984, Trends in Neurosciences.

[4]  A. Parent,et al.  The subcortical afferents to caudate nucleus and putamen in primate: A fluorescence retrograde double labeling study , 1983, Neuroscience.

[5]  M. Posner,et al.  Selective attention and cognitive control , 1987, Trends in Neurosciences.

[6]  T. Yin,et al.  Subcortical projections of the inferior parietal cortex (area 7) in the stump‐tailed monkey , 1984, The Journal of comparative neurology.

[7]  E. T. Rolls,et al.  Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum , 1984, Brain Research.

[8]  P. Goldman-Rakic,et al.  Organization of the nigrothalamocortical system in the rhesus monkey , 1985, The Journal of comparative neurology.

[9]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. , 1972, Journal of neurophysiology.

[10]  P. Buser,et al.  Single unit recording in the caudate nucleus during sessions with elaborate movements in the awake monkey. , 1974, Brain research.

[11]  D. Robinson,et al.  Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. , 1978, Journal of neurophysiology.

[12]  G. V. Van Hoesen,et al.  Widespread corticostriate projections from temporal cortex of the rhesus monkey , 1981, The Journal of comparative neurology.

[13]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. , 1983, Journal of neurophysiology.

[14]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. , 1983, Journal of neurophysiology.

[15]  K. Akert,et al.  Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique , 1977, The Journal of comparative neurology.

[16]  F. Mettler EFFECTS OF BILATERAL SIMULTANEOUS SUBCORTICAL LESIONS IN THE PRIMATE , 1945 .

[17]  D. B. Bender,et al.  Retinotopic organization of macaque pulvinar. , 1981, Journal of neurophysiology.

[18]  R. Wurtz Visual receptive fields of striate cortex neurons in awake monkeys. , 1969, Journal of neurophysiology.

[19]  J. T. Murphy,et al.  The role of the basal ganglia in controlling a movement initiated by a visually presented cue , 1980, Brain Research.

[20]  M. Kimura The role of primate putamen neurons in the association of sensory stimuli with movement , 1986, Neuroscience Research.

[21]  D. Denny-Brown,et al.  The role of the basal ganglia in the initiation of movement. , 1976, Research publications - Association for Research in Nervous and Mental Disease.

[22]  S. Thorpe,et al.  Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus , 1983, Behavioural Brain Research.

[23]  M. Goldberg,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. , 1981, Journal of neurophysiology.

[24]  M. Schlag-Rey,et al.  Visuomotor functions of central thalamus in monkey. II. Unit activity related to visual events, targeting, and fixation. , 1984, Journal of neurophysiology.

[25]  D. M. Feeney,et al.  Sensory neglect after lesions of substantia nigra or lateral hypothalamus: Differential severity and recovery of function , 1979, Brain Research.

[26]  P. E. Roland,et al.  Metabolic measurements of the working frontal cortex in man , 1984, Trends in Neurosciences.

[27]  Elsevier Biomedical Press RESPONSES OF STRIATAL NEURONS IN THE BEHAVING MONKEY. 1. HEAD OF THE CAUDATE NUCLEUS , 1983 .

[28]  B. Fischer,et al.  Peripheral attention versus central fixation: Modulation of the visual activity of prelunate cortical cells of the rhesus monkey , 1985, Brain Research.

[29]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

[30]  E. Rolls,et al.  Functional subdivisions of the temporal lobe neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  G. Krauthamer Sensory Functions of the Neostriatum , 1979 .

[32]  T. Ono,et al.  Caudate unit activity during operant feeding behavior in monkeys and modulation by cooling prefrontal cortex , 1984, Behavioural Brain Research.

[33]  T. Ljungberg,et al.  Sensory inattention produced by 6-hydroxydopamine-induced degeneration of ascending dopamine neurons in the brain , 1976, Experimental Neurology.

[34]  R. Wurtz,et al.  Enhancement of visual responses in monkey striate cortex and frontal eye fields. , 1976, Journal of neurophysiology.

[35]  M E Goldberg,et al.  Frontal eye field efferents in the macaque monkey: I. Subcortical pathways and topography of striatal and thalamic terminal fields , 1988, The Journal of comparative neurology.

[36]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.