Previous ablation studies in monkeys suggest that prefrontal cortex is involved in a wide range of learning and memory tasks. However, monkeys with crossed unilateral lesions of frontal and temporal cortex are unimpaired at concurrent object-reward association learning but are impaired at conditional learning and the implementation of memory-based performance rules. We trained seven monkeys preoperatively on an associative learning task that required them to associate objects embedded in unique complex scenes with reward. Three monkeys then had crossed unilateral lesions of frontal and inferior temporal cortex and the remaining monkeys had bilateral prefrontal cortex ablation. Both groups were severely impaired postoperatively. These results show that both bilateral prefrontal cortex ablation and frontal-temporal disconnection impair associative learning for objects embedded in scenes. The results provide evidence that the function of frontal-temporal interactions in memory is not limited to conditional learning tasks and memory-dependent performance rules. We propose that rapid object-in-place learning requires the interaction of frontal cortex with inferotemporal cortex because visual object and contextual information which is captured over multiple saccades must be processed as a unique complex event that is extended in time. The present results suggest a role for frontal-temporal interaction in the integration of visual information over time.
It is well established that the responses of neurons in the lateral geniculate nucleus (LGN) can be modulated by feedback from visual cortex, but it is still unclear how cortico-geniculate afferents regulate the flow of visual information to the cortex in the primate. Here we report the effects, on the gain of LGN neurons, of differentially stimulating the extraclassical receptive field, with feedback from the striate cortex intact or inactivated in the marmoset monkey, Callithrix jacchus. A horizontally oriented grating of optimal size, spatial frequency, and temporal frequency was presented to the classical receptive field. The grating varied in contrast (range: 0–1) from trial to trial, and was presented alone, or surrounded by a grating of the same or orthogonal orientation, contained within either a larger annular field, or flanks oriented either horizontally or vertically. V1 was ablated to inactivate cortico-geniculate feedback. The maximum firing rate of LGN neurons was greater with V1 intact, but was reduced by visually stimulating beyond the classical receptive field. Large horizontal or vertical annular gratings were most effective in reducing the maximum firing rate of LGN neurons. Magnocellular neurons were most susceptible to this inhibition from beyond the classical receptive field. Extraclassical inhibition was less effective with V1 ablated. We conclude that inhibition from beyond the classical receptive field reduces the excitatory influence of V1 in the LGN. The net balance between cortico-geniculate excitation and inhibition from beyond the classical receptive field is one mechanism by which signals relayed from the retina to V1 are controlled.
Macaque monkeys learned a strategy task in which two groups of visual objects needed to be treated differently, one with persistent and one with sporadic object choices, to obtain food rewards. After preoperative training, they were divided into two surgical groups of three monkeys each. One group received crossed unilateral removals of frontal cortex and inferior temporal cortex (IT x FC) and were severely impaired in performing the strategy task. The other group received bilateral transection of anterior temporal stem, amygdala, and fornix (TS+AM+FX) and were unimpaired in performing the strategy task. Subsequently the same animals were tested in visual object-reward association learning. Here, confirming previous results, group IT x FC was unimpaired, whereas group TS+AM+FX was severely impaired. The results show that the amnesic effects of TS+AM+FX cannot be generally attributed to the partial temporal-frontal disconnection that this lesion creates, and therefore support the hypothesis that the amnesic effects of this lesion are caused primarily by the disconnection of temporal cortex from ascending inputs from the basal forebrain. The results also show that temporal-frontal interaction in strategy implementation does not require those routes of temporal-frontal interaction that are interrupted in TS+AM+FX, and therefore support the hypothesis that projections to other posterior cortical areas allow temporal and frontal cortex to interact with each other by multisynaptic corticocortical routes in strategy implementation.
Episodic memory in humans is the conscious recollection of a past event. Animal models of episodic-like memory assess the memory for “what” happened, “where” it happened, and either “when” it happened, or in “which” context it happened, although recollection on such tasks is often difficult to measure. Here we present the first evidence of successful recollection of a past event in a rat in a task which is easily performed, requires little training, and is easily adaptable for other commonly used laboratory species.
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