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W A Suzuki

Publications and source records attributed to W A Suzuki.

14 recordsLinked to original sources

Where are the perirhinal and parahippocampal cortices? A historical overview of the nomenclature and boundaries applied to the primate medial temporal lobe.

Strong evidence has emerged over the last 15 years showing that the perirhinal and parahippocampal cortices play an important role in normal memory function. Despite our progress in understanding the mnemonic functions of these areas, controversy still exists concerning the precise location of the boundaries of these areas in the primate brain. To provide a context for understanding the current discrepancies in the literature, we present a historical overview of the different boundary schemes and nomenclatures that have been applied to the medial temporal lobe cortices in both humans and nonhuman primates. We describe how the boundaries and the names applied to these regions have evolved over time, starting with the classic cytoarchitectonisists working in the early 1900s, and ending with the various schemes being used in the contemporary literature. We show that the current controversies concerning the boundaries of the perirhinal and parahippocampal cortices can be traced directly to the classic cytoarchitectonic literature.

Anatomy↗

The hippocampus and memory: a comparative and ethological perspective.

During the past year, considerable progress has been made in our understanding of the wide-ranging functions of the hippocampus. Highlights include the development of new tasks with which to assess spatial/topographic memory in humans and monkeys, novel tests of relational memory in rats, and episodic-like memory tasks in birds. In addition, novel theories of hippocampal function have been developed that are notable for their applicability to both humans and animal models.

Animals↗

The neurophysiology of memory.

How do the structures of the medial temporal lobe contribute to memory? To address this question, we examine the neurophysiological correlates of both recognition and associative memory in the medial temporal lobe of humans, monkeys, and rats. These cross-species comparisons show that the patterns of mnemonic activity observed throughout the medial temporal lobe are largely conserved across species. Moreover, these findings show that neurons in each of the medial temporal lobe areas can perform both similar as well as distinctive mnemonic functions. In some cases, similar patterns of mnemonic activity are observed across all structures of the medial temporal lobe. In the majority of cases, however, the hippocampal formation and surrounding cortex signal mnemonic information in distinct, but complementary ways.

Animals↗

Hierarchical organization of cognitive memory.

This paper addresses the question of the organization of memory processes within the medial temporal lobe. Evidence obtained in patients with late-onset amnesia resulting from medial temporal pathology has given rise to two opposing interpretations of the effects of such damage on long-term cognitive memory. One view is that cognitive memory, including memory for both facts and events, is served in a unitary manner by the hippocampus and its surrounding cortices; the other is that the basic function affected in amnesia is event memory, the memory for factual material often showing substantial preservation. Recent findings in patients with amnesia resulting from relatively selective hippocampal damage sustained early in life suggest a possible reconciliation of the two views. The new findings suggest that the hippocampus may be especially important for event as opposed to fact memory, with the surrounding cortical areas contributing to both. Evidence from neuroanatomical and neurobehavioural studies in monkeys is presented in support of this proposal.

Amnesia↗

Object and place memory in the macaque entorhinal cortex.

Lesions of the entorhinal cortex in humans, monkeys, and rats impair memory for a variety of kinds of information, including memory for objects and places. To begin to understand the contribution of entorhinal cells to different forms of memory, responses of entorhinal cells were recorded as monkeys performed either an object or place memory task. The object memory task was a variation of delayed matching to sample. A sample picture was presented at the start of the trial, followed by a variable sequence of zero to four test pictures, ending with a repetition of the sample (i.e., a match). The place memory task was a variation of delayed matching to place. In this task, a cue stimulus was presented at a variable sequence of one to four "places" on a computer screen, ending with a repetition of one of the previously shown places (i.e., a match). For both tasks, the animals were rewarded for releasing a bar to the match. To solve these tasks, the monkey must 1) discriminate the stimuli, 2) maintain a memory of the appropriate stimuli during the course of the trial, and 3) evaluate whether a test stimulus matches previously presented stimuli. The responses of entorhinal cortex neurons were consistent with a role in all three of these processes in both tasks. We found that 47% and 55% of the visually responsive entorhinal cells responded selectively to the different objects or places presented during the object or place task, respectively. Similar to previous findings in prefrontal but not perirhinal cortex on the object task, some entorhinal cells had sample-specific delay activity that was maintained throughout all of the delay intervals in the sequence. For the place task, some cells had location-specific maintained activity in the delay immediately following a specific cue location. In addition, 59% and 22% of the visually responsive cells recorded during the object and place task, respectively, responded differently to the test stimuli according to whether they were matching or non-matching to the stimuli held in memory. Responses of some cells were enhanced to matching stimuli, whereas others were suppressed. This suppression or enhancement typically occurred well before the animals' behavioral response, suggesting that this information could be used to perform the task. These results indicate that entorhinal cells receive sensory information about both objects and spatial locations and that their activity carries information about objects and locations held in short-term memory.

Analysis of Variance↗

Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys.

Neuroanatomical studies in macaque monkeys have demonstrated that the perirhinal and parahippocampal (PRPH) cortices are strongly interconnected with the hippocampal formation. Recent behavioral evidence indicates that these cortical regions are importantly involved in normal recognition memory function. The PRPH cortices are also interconnected with the amygdaloid complex, although comparatively little is known about the precise topography of these connections. We investigated the topographic organization of reciprocal connections between the amygdala and the PRPH cortices by placing anterograde and retrograde tracers throughout these three regions. We found that there was an organized arrangement of connections between the amygdala and the PRPH cortices and that the deep (lateral, basal, and accessory basal) nuclei of the amygdaloid complex were the source of most connections between the amygdala and the PRPH cortices. The temporal polar regions of the perirhinal cortex had the strongest and most widespread interconnections with the amygdala. Connections from more caudal levels of the perirhinal cortex had a more discrete pattern of termination. Perirhinal inputs to the amygdala terminated primarily in the lateral nucleus, the magnocellular and parvicellular divisions of the basal nucleus, and the magnocellular division of the accessory basal nucleus. Return projections originated predominately in the lateral nucleus, the intermediate and parvicellular divisions of the basal nucleus, and the magnocellular division of the accessory basal nucleus. The interconnections between the amygdala and the parahippocampal cortex were substantially less robust than those with the perirhinal cortex and mainly involved the basal nucleus. Area TF was more strongly interconnected with the amygdala than was area TH. Input from the parahippocampal cortex terminated predominantly in the lateral half of the parvicellular division of the basal nucleus but also to a lesser extent in the magnocellular division of the basal nucleus and the lateral nucleus. Return projections originated predominantly in the magnocellular division of the basal nucleus and were directed almost exclusively to area TF.

Amygdala↗

The anatomy, physiology and functions of the perirhinal cortex.

The perirhinal cortex is a polymodal association area that contributes importantly to normal recognition memory. A convergence of recent findings from lesion and electrophysiological studies has provided new evidence that this area participates in an even broader range of memory functions than previously thought, including associative memory and emotional memory, as well as consolidation functions. These results are consistent with neuroanatomical research showing that this area has strong and reciprocal connections with widespread cortical sensory areas and with other memory-related structures, including the hippocampal formation and amygdala.

Animals↗

Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents.

Neuropsychological studies have recently demonstrated that the macaque monkey perirhinal (areas 35 and 36) and parahippocampal (areas TH and TF) cortices contribute importantly to normal memory function. Unfortunately, neuroanatomical information concerning the cytoarchitectonic organization and extrinsic connectivity of these cortical regions is meager. We investigated the organization of cortical inputs to the macaque monkey perirhinal and parahippocampal cortices by placing discrete injections of the retrograde tracers fast blue, diamidino yellow, and wheat germ agglutinin conjugated to horseradish peroxidase throughout these areas. We found that the macaque monkey perirhinal and parahippocampal cortices receive different complements of cortical inputs. The major cortical inputs to the perirhinal cortex arise from the unimodal visual areas TE and rostral TEO and from area TF of the parahippocampal cortex. The perirhinal cortex also receives projections from the dysgranular and granular subdivisions of the insular cortex and from area 13 of the orbitofrontal cortex. In contrast, area TF of the parahippocampal cortex receives its strongest input from more caudal visual areas V4, TEO, and caudal TE, as well as prominent inputs from polymodal association cortices, including the retrosplenial cortex and the dorsal bank of the superior temporal sulcus. Area TF also receives projections from areas 7a and LIP of the posterior parietal lobe, insular cortex, and areas 46, 13, 45, and 9 of the frontal lobe. As with area TF, area TH receives substantial projections from the retrosplenial cortex as well as moderate projections from the dorsal bank of the superior temporal sulcus; unlike area TF, area TH receives almost no innervation from areas TE and TEO. It does, however, receive relatively strong inputs from auditory association areas on the convexity of the superior temporal gyrus.

Animals↗

Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices.

The perirhinal and parahippocampal cortices constitute the major sources of cortical input to the monkey entorhinal cortex. Neuropsychological studies have shown that these three cortical regions contribute in an important way to normal memory function. We have investigated the topographic and laminar organization of the reciprocal projections between the entorhinal cortex and these two adjacent cortical areas by placing anterograde and retrograde tracers in all three regions. There were three major findings. First, the perirhinal and parahippocampal cortices have distinct but partially overlapping interconnections with the entorhinal cortex. The perirhinal cortex tends to be interconnected with the rostral two-thirds of the entorhinal cortex while the parahippocampal cortex tends to be interconnected with approximately the caudal two-thirds of the entorhinal cortex. Second, the degree of reciprocity of the interconnections of the entorhinal cortex with the perirhinal and parahippocampal cortices differs. The parahippocampal/entorhinal connections have a high degree of reciprocity. In contrast, the degree of reciprocity of the perirhinal/entorhinal interconnections varies depending on the mediolateral position within the perirhinal cortex; medial portions of the perirhinal cortex exhibit a higher degree of reciprocity with the entorhinal cortex than lateral portions. Third, the projections from the perirhinal and parahippocampal cortices to the entorhinal cortex resemble a feedforward projection, while the projections from the entorhinal cortex to the perirhinal and parahippocampal cortices resemble a feedback projection pattern.

Animals↗

Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities.

Compared to normal animals, monkeys with bilateral lesions of the perirhinal and parahippocampal cortices (PRPH lesion) were impaired on both a visual and a tactual version of the delayed nonmatching to sample task. In addition, the memory deficit was long-lasting, as indicated by the finding of a significant deficit when the visual version of the delayed nonmatching to sample task was readministered approximately 2 years after surgery. Animals with PRPH lesions performed normally on discrimination tasks in the visual and tactual modalities. Multimodal and long-lasting memory impairments are defining characteristics of human medial temporal lobe amnesia. Accordingly, these results demonstrate important parallels between the memory deficit associated with PRPH lesions and human medial temporal lobe amnesia. These data, taken together with previous findings, suggest that the perirhinal and parahippocampal cortices play an important role in memory function and that these cortical areas are critical components of the medial temporal lobe memory system.

Animals↗

Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE.

We determined the cortical regions that project directly to the CA1 field of the monkey hippocampus by injecting the retrograde tracers Fast blue, Diamidino yellow or WGA-HRP into CA1 and examining the distribution of labeled cells. In the temporal lobe, large numbers of retrogradely labeled cells were observed in the perirhinal and parahippocampal cortices. Only an occasional labeled cell, however, was observed in the unimodal visual area TE. Additional projections to CA1 arose in the dorsal bank of the superior temporal sulcus, in the rostral and retrosplenial portions of the cingulate cortex, in the agranular insular cortex, and in the caudal orbitofrontal cortex.

Amidines↗

Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment.

In monkeys, bilateral damage to the medial temporal region produces severe memory impairment. This lesion, which includes the hippocampal formation, amygdala, and adjacent cortex, including the parahippocampal gyrus (the H+A+ lesion), appears to constitute an animal model of human medial temporal lobe amnesia. Reexamination of histological material from previously studied monkeys with H+A+ lesions indicated that the perirhinal cortex had also sustained significant damage. Furthermore, recent neuroanatomical studies show that the perirhinal cortex and the closely associated parahippocampal cortex provide the major source of cortical input to the hippocampal formation. Based on these 2 findings, we evaluated the severity of memory impairment in a group of monkeys that received bilateral lesions limited to the perirhinal cortex and parahippocampal gyrus (the PRPH lesion). The performance of the PRPH group was compared with that of monkeys with H+A+ lesions, who had been studied previously, and with a group of normal monkeys. Monkeys with PRPH lesions were severely impaired on 3 amnesia-sensitive tasks: delayed nonmatching to sample, object retention, and 8-pair concurrent discrimination. On pattern discrimination, a task analogous to ones that amnesic patients perform well, monkeys in the PRPH group performed normally. Overall, monkeys with PRPH lesions were as impaired or more impaired than the comparison group of monkeys with H+A+ lesions. These and other recent findings (Zola-Morgan et al., 1989b) suggest that the severe memory impairment in monkeys and humans associated with bilateral medial temporal lesions results from damage to the hippocampal formation and adjacent, anatomically related cortex, not from conjoint hippocampus-amygdala damage.

Amygdala↗