Summary
The inferotemporal cortex of primates plays a prominent role in the learning and retention of visual form discriminations. In this experiment we investigated the role of inferotemporal (IT) cortex in the discrimination of two-dimensional forms defined by motion cues. Six monkeys were trained to a criterion level of performance on two form-from-motion problems. Three of these animals received complete bilateral lesions of IT cortex, while the other three served as unoperated controls. All animals were then retrained to criterion to evaluate the effects of IT lesions on the retention of form-from-motion learning. Compared with the control group, the lesion group was significantly impaired on both problems. Following retention testing, we trained both groups of monkeys on two new form-from-motion problems to investigate the effects of IT lesions on acquisition rates for new learning. The lesion group performed well on the new problems; the learning rates of the operated and control groups were not significantly different. When forms were defined by luminance cues, monkeys with IT lesions, like those in previous studies, were impaired both for retention and for acquisition. These findings indicate that the anterograde effects of IT lesions on learning new form discriminations are less severe for forms defined by motion cues than for forms defined by luminance cues. However, the retrograde effects of IT lesions on retention are severe for forms defined by either cue.
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References
Bagshaw MH, Mackworth NH, Pribram KH (1970) The effect of inferotemporal cortex ablations on eye movements of monkeys during discrimination training. Int J Neurosci 1:153–158
Baizer JS, Robinson DL, Dow BM (1977) Visual responses of area 18 neurons in awake, behaving monkey. J Neurophysiol 40:1024–1037
Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to inferior temporal and posterior parietal cortex in macaques. J Neurosci 11:168–190
Battersby WS, Bender MB, Pollack M, Kahn RL (1956) Unilateral “spatial agnosia” (“inattention”) in patients with cerebral lesions. Brain 79:68–93
Benevento LA, Rezak M (1976) The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatta): an autoradiographic study. Brain Res 108:1–24
Bonin GV, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana Illinois
Boussaoud D, Ungerleider LG, Desimone R (1990) Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J Comp Neurol 296:462–495
Brain WR (1941). Form of visual disorientation resulting from lesions of right cerebral hemisphere. Proc R Soc Med 34:771–776
Britten KH, Newsome WT, Saunders RC (1989) Effects of inferotemporal cortex lesions on pattern-from-motion discrimination in monkeys. Soc for Neurosc Abstr 15:1256
Bruce CJ, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophys 46:369–384
Burkhalter A, Van Essen DC (1986) Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey. J Neurosci 6:2327–2351
Chow KL (1950) A retrograde cell degeneration study of the cortical projection field of the pulvinar in the monkey. J Comp Neurol 93:313–340
Chow KL (1954) Lake of behavioral effects following lesions of some thalamic association nuclei in monkey. AMA Arch Neurol Psychiat 71:762–771
Cole M, Schutta HS, Warrington EK (1962) Visual disorientation in homonymous half-fields. Neurology 12:257–263
Cowey A (1979) Cortical maps and visual perception. Q J Exp Psychol 31:1–17
Cowey A, Weiskrantz L (1968) Varying spatial separation of cues, response, and reward in visual discrimination learning in monkeys. J Comp Phys Psych 11:220–224
Damasio AR, Damasio H, Van Hoesen GW (1982) Prosopagnosia: anatomic basis and behavioral mechanisms. Neurology 32:331–341
Dean P (1976) Effects of inferotemporal lesions on the behavior of monkeys. Psychol Bull 83:41–71
Dean P, Weiskrantz L (1974) Loss of preoperative habits in rhesus monkeys with inferotemporal lesion: recognition failure or relearning deficit? Neuropsychologia 12:299–311
Desimone R, Schein SJ (1987) Visual properties of neurones in area V4 of the macaque: sensitivity to stimulus form. J Neurophysiol 57:835–868
Ettlinger G, Iwai I, Mishkin M, Rosvold H (1968) Visual discrimination in monkey following serial ablation of inferotemporal and preoccipital cortex. J Comp Phys Psych 65:110–117
Felleman DJ, Van Essen DC (1987). Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. J Neurophys 57:889–920
Gross CG (1973) Inferotemporal cortex and vision. Prog Physiol Psychol 5:77–123
Heilman KM, Pandya DN, Geschwind N (1970) Trimodal inattention following parietal lobe ablations. Trans Am Neurol Assoc 95:259–261
Heilman KM, Valenstein E (1979) Clinical neuropsychology. Oxford University Press, New York
Holmes EJ, Gross CG (1984) Effects of inferior temporal lesions on discrimination of stimuli differing in orientation. J Neurosci 4:3063–3068
Holmes G (1918) Disturbances of visual orientation. Br J Opthal 2:449
Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535–538
Kimura D (1963) Right temporal-lobe damage: perception of unfamiliar stimuli after damage. Arch Neurol 8:264–271
Lawler KA, Cowey A (1987) On the role of posterior parietal and prefrontal cortex in visuospatial perception and attention. Exp Br Res 65:695–698
Malpeli JG, Baker FH (1975) The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. J Comp Neurol 161:569–594
Maunsell JHR, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Ann Rev Neurosci 10:363–401
Maunsell JHR, Van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical heirarchy in the macaque monkey. J Neurophysiol 3:2563–2586
Meadows JC (1974) The anatomical basis of prosopagnosia. J Neurol Neurosurg Psychiatr 37:489–501
Merigan WH (1980) Temporal modulation sensitivity of macaque monkeys. Vision Res 20:953–959
Mishkin M, Lewis ME, Ungerleider LG (1982). Equivalence of parieto-preoccipital subareas for visuospatial ability in monkeys. Behav Brain Res 6:41–55
Mishkin M, Ungerleider LG (1982) Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behav Brain Res 6:57–77
Mishkin M, Weiskrantz L (1958) Effects of delaying reward on visual discrimination learning with frontal lesions. J Comp Phys Psychol 3:276–281
Nakayama K, Loomis JM (1974) Optical velocity patterns, velocity-sensitive neurons, and space perception: a hypothesis. Perception 3:63–80
Newsome WT, Pare EB (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8:2201–2211
Orban GA, Kennedy H, Bullier J (1986) Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: Influence of eccentricity. J Neurophysiol 56:462–480
Oscar-Berman M, Heywood S, Gross CG (1974) The effects of posterior cortical lesions on eye orientation during visual discrimination by monkeys. Neuropsychologia 12:175–182
Pasternak T, Horn KM, Maunsell JHR (1989) Deficits in speed discrimination following lesions of the lateral suprasylvian cortex in the cat. Vis Neurosci 3:365–375
Perrett DI (1985) Visual analysis of body movements by neurons in the temporal cortex of the macaque monkey: a preliminary report. Behav Br Res 16:153–170
Pohl W (1973) Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. J Comp Physiol Psychol 82:227–239
Ratcliff G, Davies-Jones AB (1972) Defective visual localization in focal brain wounds. Brain 95:49–60
Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145
Rosene DL, Roy NJ, Davis BJ (1986) A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. J Histochem Cytochem 34:1301–1315
Siqueira EB (1965) The temporo-pulvinar connections in the rhesus monkey. Arch Neurol 13:321–330
Trojanowski JQ, Jacobson S (1976) Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. J Comp Neurol 169:371–392
Ungerleider LG, Christensen CA (1977) Pulvinar lesions produce abnormal eye movements during visual discrimination training. Brain Res 136:189–196
Ungerleider LG, Desimone R (1986) Cortical connections of visual area MT in the macaque. J Comp Neurol 248:190–222
Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJ (ed) Analysis of visual behavior. MIT Press, Cambridge Mass, pp 549–580
Van Essen DC (1985) Functional organization of primate visual cortex. In: Peters A, Jones EG (ed) Cerebral cortex. Plenum Press, New York, pp 259–329
Van Essen DC, Felleman DJ, De Yoe EA, Olavierra J, Knierim J (1990) Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. Cold Spring Harbor Symp Quant Biol 55. Cold Spring Harbor Laboratory, pp 679–696
Wallach H, O'Connell DN (1953) The kinetic depth effect. J Exp Psychol 45:205–217
Zeki SM (1978) Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. J Physiol 277:273–290
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Britten, K.H., Newsome, W.T. & Saunders, R.C. Effects of inferotemporal cortex lesions on form-from-motion discrimination in monkeys. Exp Brain Res 88, 292–302 (1992). https://doi.org/10.1007/BF02259104
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DOI: https://doi.org/10.1007/BF02259104