James A. Horel

The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold.

Cold was used to suppress the function of subdivisions of the inferotemporal cortex. Three cryodes were placed bilaterally, one over the lower bank of the superior temporal sulcus (sts), one over the middle temporal gyrus (mtg) and one over the inferior temporal gyrus (itg). The animals were tested with delayed match-to-sample (DMS) and simultaneous visual discriminations. The DMS required the animal to recall a projected image of an object over delays of 0, 15, 30 and 45 s. The 3 cryodes were cooled separately during the performance of the DMS and only itg cooling produced a deficit. This was compared to the effects of ablative bilateral lesions; damage to itg but not mtg disrupted performance of DMS. The greatest deficit was in an animal with a small lesion in the ventral pole and anterior extreme of itg. Cooling individual cryodes was without effect on a discrimination between horizontal and vertical stripes, but produced a significant deficit from each of the 3 placements on a discrimination between monkey faces. Chance performance on all visual discriminations resulted from cooling all cryodes. Unilateral cooling of all cryodes produced significant effects on the face discrimination, but there was no significant difference between the two sides in the severity of the deficit.

Some Comments on the Special Cognitive Functions Claimed for the Hippocampus

This paper challenges the idea that memory is the special function of any single brain structure, an idea that developed from clinical cases of amnesia that had lesions in and around the hippocampus. There are many instances of amnesia and other evidence of memory functions in brain areas that do not involve the hippocampus. The evidence that medial temporal lobe lesions in animals produce uncontaminated memory deficits is reviewed and rejected, as well as the evidence that the memory task used in these experiments has any special relationship to the hippocampus. It is proposed that memory is not the function of any one structure, but is a part of local neuronal operations carried out in all cortical areas where the information to be remembered is processed and perceived. If this suggestion is correct, then a local lesion will cause a loss of local function and the memory for that function.

Retrieval of color and form during suppression of temporal cortex with cold

Five cryodes were implanted on each side over the dorsal aspect of inferotemporal cortex (TEd) of three monkeys. They were trained on a form discrimination and three color discriminations. Suppression of TEd with cold disrupted retrieval of the color, but not the form discriminations. The animals could find the colors in a background of shifting values of gray, indicating that the suppression did not reduce their color perception to gray. They initially had great difficulty matching red to red and green to green, although that recovered with experience. The animals tended to respond to one or the other of the colors, indicating that they could perceive and discriminate them, but, either lost information about the correct stimulus, or something from past experience was interfering with performance. We suggested that cooling TEd suppresses new and recent learning of color discriminations, but it does not suppress some previous experience that intrudes upon performance of new tasks. TEd might contain episodic information about colors necessary for performance of the immediate task.

Local and global perception examined by reversible suppression of temporal cortex with cold

We placed cryodes over both sides of the dorsal inferotemporal cortex (TEd) in three monkeys in order to suppress its functions during perception of compound visual images. We used three pairs of images in a concurrent visual discrimination: 1. Congruent pair, a large T made of small Ts and a large 7 made of small 7s with response to the large 7 rewarded. 2. Incongruent pair, a T made of small 7s and a 7 made of small Ts with response to the large 7 rewarded. 3. Random pair, a scattering of small Ts in one stimulus and small 7s in the other with response to the small 7 rewarded. If TEd processes the global but not the local elements of a visual figure, animals with TEd suppressed should see only the local figures and they would fail only on the incongruent stimulus. Alternatively, if TEd processed the local, but not the global elements, they should fail only on the scattered small figures where there was no global element as a cue. Finally, if TEd suppression impairs discrimination of forms, they should be impaired on all the figures because they were the same form, but different size. We found that during TEd suppression, the animals failed on the scattered small elements, but not on the global figures formed of the small elements.

Retention deficits produced in monkeys with reversible cold lesions in the prestriate cortex

Cryodes were implanted over the prelunate and fusiform gyri in 4 monkeys. The intention was to block the prestriate projection to the inferotemporal cortex (IT). Cooling this cortex produced deficits that were completely reversed by removing the cold. The deficits appeared in the recall of visual discriminations that were learned prior to the application of the cold, but new discriminations were learned during cooling at the same rate as in control animals. This closely resembles the results of ablation experiments in this same cortex. There was no deficit when cooling this area on a delayed match-to-sample (DMS) task that required the animals to hold visual information over delays of 10 or 45 s. However, performance was close to chance during cooling when the delays were 6 min. With this long delay, when cooling was done separately at sample when the stimulus is received, or at match when the information is recalled, a significant deficit occurred only at match. The results are consistent with the suggestion that this area is involved in retrieval of visual information from long-term memory.

Perception, learning and identification studied with reversible suppression of cortical visual areas in monkeys.

We use cold to reversibly suppress cortical areas involved in visual perception, learning and retrieval and we found a localization of functions essential for performance of delayed match-to-sample (DMS) in anterior ventral temporal cortex, we call ventral TE (TEv). We also found a visual input for this area that is separate from the one going to the heart of inferotemporal cortex and suppressing this input also impairs performance of DMS. Suppressing the dorsal half of TE (TEd) disrupts retrieval of some, but not all complex images, and different images are disrupted in different animals. This variability within and between animals is extreme, with perfect performance on some complex images and below chance on others. We suggested that TEd represents some, but not all elements of the images. In attempting to discover what those elements might be, we found that TEd suppression disrupts the perception of small figures, but not the larger figures that they compose. We also found that it impaired the discrimination and matching of colors, without impairing the ability to detect and differentiate hues. We proposed that TEd represents the details and colors of things, but not global figures. Also, complex objects do not have a representation in one area, rather its representation involves the entire visual system, including TE with different elements of the image represented in different parts.

Retrieval of a face discrimination during suppression of monkey temporal cortex with cold

Cells in the monkey temporal cortex that respond selectively to faces suggest that monkeys might have a brain structure similar to that in humans where lesions produce prosopagnosia, but effects of lesions on retrieval of face discriminations have been ambiguous in monkeys. It is possible that the stimuli in the monkey experiments were contaminated with non-face elements that could be discriminated by other parts of the visual system. In this experiment we modified the image of a monkey face creating two faces that were identical except for their internal features. We trained monkeys to discriminate these faces and then reversibly suppressed the inferotemporal cortex with cold and tested their ability to recall them. Cooling the temporal cortex produced a severe impairment in retrieval of the discrimination that remained constant across six 40-trial replications.

Retrieval of active and inactive visual discriminations while temporal cortex is suppressed with cold

While local cooling of inferotemporal cortex (IT) impairs new visual learning, it has little effect on recall. However, in visual discriminations, there is typically extensive exposure to the stimuli before cortical inactivation. Perhaps if recall was prevented before suppression, it would fail during suppression. Three animals with cryodes covering a major part of IT were trained on two face discriminations. They were then run on one of these discriminations for 3 days to create the expectation that the task would be continued with the same stimuli, and on the 4th day, they were started with these stimuli, but after cold suppression, they were switched to a discrimination that they should not have anticipated. IT suppression prevented recall of the discrimination that had not been pre-exposed; performance dropped to chance and stayed there for 50 trials. When they were switched back to the initial pair, performance returned nearly to normal. The experiment was repeated with the role of anticipated and unanticipated stimuli reversed. It was suggested that pre-exposure to the discrimination created the expectation that the same stimuli would continue to be used, and induced information about them to be copied from IT into prestriate cortex.

The effects of number of stimuli and prior exposure on performance of concurrent visual discriminations during suppression of inferotemporal cortex with cold

The visual part of the temporal cortex, cytoarchitectural area TE has been split into dorsal (TEd) and ventral (TEv) subdivisions. TE has long been associated with the identification of objects. However, in order to explain retrieval deficits with suppression of prestriate cortex, but not with suppression of TE, we hypothesized that object identification might take place in a working memory in the prestriate cortex upstream from TE. Exposure to the stimuli before suppressing TEd was hypothesized to cause its contribution to be relayed to prestriate cortex in anticipation of further work with them. This predicts that during TEd suppression there is a loss of access to some long-term visual memory, and without that access, large numbers of stimuli should overwhelm the limited capacity working memory. It also predicts that prior exposure to stimuli should protect them from loss during TEd suppression. We challenged these predictions in two experiments. In the first, we tested the animals on three concurrent discriminations requiring them to retrieve 8 pairs of stimuli for each one. The animals performed well on some of the discriminations during TEd suppression, but failed on others, which is consistent with the prediction. Also, different animals failed with different stimuli. However, when we tested with only the failed discriminations, they still did badly with one or two pairs, which is not consistent with the prediction. In the second experiment, we tested them with 1, 4, 7 or 10 pairs of visual discriminations drawn from a set of 23 the animals had learned. Half of the discriminations were presented immediately before suppression and half were not.(ABSTRACT TRUNCATED AT 250 WORDS)