Impact of learning on representation of parts and wholes in monkey inferotemporal cortex

Abstract

Visual object recognition is thought to depend on experienceinduced changes in inferotemporal (IT) cortex, such that neurons become more selective for (or more responsive to) learned images [1][2][3][4] . This view is consistent with evidence showing that lesions in IT interfere with pattern recognition 5,6 , that neurons in IT are pattern-selective 5,6 and that IT is a site of experience-dependent plasticity. Plasticity has been shown in IT by the use of three approaches: (i) repeated exposure to a stimulus over a short period of time leads to a decline in response strength 7-10 , (ii) prolonged training on a visual paired associate task results in the emergence of neurons that are responsive to both members of the pair [11][12][13] and (iii) discrimination training. Training monkeys to discriminate among images is thought to induce changes in the strength and selectivity of neuronal responses to those images, but studies to date have produced contradictory and inconclusive results. On the one hand, some neurons seem to become markedly selective for learned images. For example, in a study of monkeys trained to discriminate among wire objects 14,15 , several units showed "a remarkable selectivity" for individual views that the monkey had learned to recognize. On the other hand, two studies involving a single day 16 or several months 17 of training do not show evidence of enhanced selectivity for images in the training set. In another study 18 , discrimination training resulted in a subtle enhancement of stimulus selectivity at the population level, but this effect was shown by comparing trained to untrained monkeys rather than by comparing responses to learned and unlearned stimuli in the same monkey. Thus, innate differences between monkeys may have contributed to the result. Finally, learned images have been reported to elicit higher firing rates than unlearned images [18][19][20] . Here we investigated the impact of visual discrimination training on neuronal responses to parts of images and to whole images in inferotemporal (IT) cortex. Monkeys were trained to discriminate among 'baton' stimuli consisting of discrete top and bottom parts joined by a vertical stem. With separate features at each end, we were able to manipulate the two parts of each baton independently. After training the monkeys, we used single-cell recording to compare neuronal responses to learned and unlearned batons. Responses to learned batons, though not enhanced in strength, were enhanced in selectivity for both individual parts and for whole batons. Whole-baton selectivity arose from a form of conjunctive encoding whereby two parts together exerted a greater influence on neuronal activity than predicted by the additive influence of each part considered individually. These results indicate a possible neural mechanism for holistic or configural effects in expert versus novice observers.An important question not addressed in previous studies is whether discrimination training enhances neuronal selectivity for whole images or for the parts...

Specialization within the ventral stream: the case for the visual word form area

“…Likewise, the binding of letters into words might be related to the representation of complex objects in IT cortex through the coactivation of neurons tuned to their elementary parts (Tsunoda et al, 2001). Binding of letters may also be based on more holistic coding, as suggested by the recent demonstration that single IT neurons develop selectivity for learned complex shapes, above and beyond what could be expected from the additive influence of their component parts (Baker et al, 2002). Such neurophysiological mechanisms may provide a neuronal basis for the acquisition of invariant visual word recognition in humans.…”

Visual word processing and experiential origins of functional selectivity in human extrastriate cortex

“…In a recent study (49), we found that 10 h of training on a novel object category produces a nearly 2-fold response to trained compared with untrained categories in some voxels in the ventral visual pathway, which was not present before training. Similarly, neurophysiological studies in nonhuman primates have found that training on discrimination and recognition of visual objects can lead to changes in the selectivity of neural responses in the inferior temporal cortex, a region critical for object recognition (50,51). Finally, experience with visual objects can lead to clustering of neurons with similar selectivity within the inferior temporal cortex (52).…”

Statistical learning of visual transitions in monkey inferotemporal cortex

“…Attentional enhancement of visual response strength in extrastriate cortex depends on the simultaneous presence of competing images elsewhere in the visual field (31,53,54). The strength of the response to an isolated foveal image is not affected by whether the monkey is processing it actively or merely is maintaining passive fixation (5,55). Nor is the strength of the response enhanced by making the image surprising through the violation of expectations other than those based on learned image-image transitional rules (56,57).…”