Masao Yukie

Connections between the medial temporal cortex and the CA1 subfield of the hippocampal formation in the Japanese monkey (Macaca fuscata).

The connections between the medial temporal cortical areas and CA1 of the hippocampus were examined in the Japanese monkey (Macaca fuscata) by means of retrograde and anterograde tract‐tracing methods with wheat germ agglutinin‐conjugated horseradish peroxidase (WGA‐HRP) and fluorescent dyes (Fast Blue and Diamidino Yellow). The posterior parahippocampal (areas TF1, TF2, and TH), perirhinal (areas 35 and 36), and ventral inferotemporal areas (areas TEav and TEpv) were reciprocally connected with CA1. Projection fibers from CA1 to the medial temporal cortical areas originated in the pyramidal cell layer, whereas those from the medial temporal cortical areas to CA1 terminated in the molecular layer. Each of these cortical areas was reciprocally connected with the entire rostrocaudal extent of CA1. However, the intensity of the connections varied along the rostrocaudal axis of CA1: areas TH and TF2 were connected most markedly with the anterior and middle parts of CA1, respectively. Areas TF, 35, 36, TEav, and TEpv were connected predominantly with the posterior part of CA1. In the coronal plane of CA1, labeled cells were located in proximal CA1 (i.e., near the prosubiculum), but not in distal CA1 (i.e., near CA2). The medial temporal cortical areas in direct reciprocal connection with CA1 were presumed to be involved in the memory system, especially in the system for declarative memory. J. Comp. Neurol. 423:282–298, 2000.

Connections between the amygdala and auditory cortical areas in the macaque monkey

Connections between the amygdala and auditory cortical areas TC, and the rostral, intermediate and caudal regions of area TA (TAr, TAi and TAc, respectively) in the macaque monkey (Macaca fuscata and Macaca nemestrina) were investigated following placements of cortical deposits of wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP). Areas TC and TAc received weak projections and these derived only from the lateral basal nucleus. Areas TAi and TAr received projections from the lateral, lateral basal and accessory basal nuclei. In contrast, corticopetal projections to the amygdala originated in areas TAi and TAr, but never in TAc or TC. The projections from areas TAi and TAr terminated only in the lateral nucleus, and in particular at the lateral part of the middle and caudal portions of the amygdala. Thus, the amygdalofugal projections to the auditory cortices are more widespread and more complex than the amygdalopetal projections of the auditory cortices. As judged from experiments in which deposits were made at different sites along the rostrocaudal axis of the auditory cortex, there was a progressive increase seen in density of the amygdala connections with more anteriorly-placed injection sites.

Laminar origin of direct projection from cortex area V1 to V4 in the rhesus monkey

Direct projection from cortex area V1 to V4 in the rhesus monkey was demonstrated by means of retrograde axonal transport of wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP). This projection originated at the layers 2 and 3 of the only representation area of central visual field (0-6 degrees) in V1 and terminated at the central representation of V4, whereas there was no projection between the extracentral representations of V1 and V4. Correlation of the present finding with the previous findings suggests that this projection is predominantly involved in the system of color information processing.

Amygdalar connections with middle and inferior temporal gyri of the monkey

The origins and terminations of the amygdalar connections with middle (ITm) and inferior temporal (ITi) gyri of inferotemporal cortex (area TE) were studied in Japanese monkeys by the horseradish peroxidase method. The ITm gyrus received a major projection from the lateral basal nucleus and a minor one from the accessory basal nucleus of the amygdala, whereas it sent a major projection to the lateral nucleus and a minor one to the lateral basal nucleus. The ITi gyrus had only minor amygdalar projections from the medial basal nucleus and to the medial basal and lateral nuclei.

Direct projections from the ventral TE area of the inferotemporal cortex to hippocampal field CA1 in the monkey.

Anterogradely labeled terminals were found densely in field CA1, but not in any other field, of the hippocampal formation following injections of horseradish peroxidase into the ventral TE area of the inferotemporal cortex, whereas no label was seen in any field of the hippocampal formation following injections into the dorsal TE area. The labeled terminals were distributed mainly in a medial part of the stratum moleculare of field CA1 throughout its rostrocaudal extent. The present finding provides the first demonstration of direct projections from the inferotemporal cortex to the hippocampal formation.

A direct projection from hippocampal field CA1 to ventral area TE of inferotemporal cortex in the monkey.

Retrogradely labeled cells were found in field CA1 of the hippocampal formation in monkeys following injections of horseradish peroxidase in ventral area TE of inferotemporal cortex. No hippocampal label was found following injections in dorsal area TE and area TEO. The findings provide the first demonstration of a direct projection from hippocampal field CA1 to area TE.

Differential thalamic connections of the posteroventral and dorsal posterior cingulate gyrus in the monkey

Previous functional studies suggest that the posterior cingulate gyrus is involved in spatial memory and its posteroventral part, in particular, is also involved in auditory memory. However, it is not clear whether the neural connections of the posteroventral part differ from those of the rest of the posterior cingulate gyrus. Here, we describe the thalamic connections of the posteroventral part of monkey area 23b (pv‐area 23b), the main component of the posteroventral posterior cingulate gyrus. We compare these thalamic connections with those of the more dorsal area 23b (d‐area 23b) and of adjoining retrosplenial areas 29 and 30. Thalamocortical projections to pv‐area 23b originate mainly from the anterior nuclei, nucleus lateralis posterior and medial pulvinar. In contrast, projections to d‐area 23b originate from the nucleus lateralis posterior, medial pulvinar, nucleus centralis latocellularis, mediodorsal nucleus and nucleus ventralis anterior and lateralis and weakly from the anterior nuclei. Projections to retrosplenial areas 29 and 30 originate from the anterior nuclei. Corticothalamic projections from pv‐area 23b terminate in the anterior and laterodorsal nuclei, nucleus lateralis posterior and medial pulvinar. Projections from d‐area 23b terminate in these nuclei as well as the nucleus ventralis anterior and lateralis. Projections from area 30 terminate mainly in the anterior nuclei and, to a lesser extent, in the medial pulvinar. These results show that the connections of pv‐area 23b differ from those of d‐area 23b or areas 29 and 30. This suggests that pv‐area 23b may play distinct functional roles in memory processes, such as spatial and auditory memory.

Neural connections of auditory association cortex with the posterior cingulate cortex in the monkey

Clinical studies have indicated that the posterior cingulate cortex is intimately involved in verbal and auditory memory. The present study was performed to obtain anatomical evidence for the above proposal. The connections of the auditory cortical areas with the posterior cingulate cortex in the macaque monkey were examined by retrograde and anterograde tracing methods using wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP). WGA-HRP was injected into either area TA, TB or TC in the superior temporal auditory cortex. Area TA was reciprocally connected with the posterior cingulate cortex, whereas areas TC and TB were not. The rostral two-thirds of area TA had major connections with the caudomedial lobule in the retrosplenial cortex (CML of Goldman-Rakic et al., 1984) and a minor one with area 23b. The caudal third of area tA was connected only with area 23b. However, neither labeled cells nor terminals were observed in areas 23a, 23c, 29, 30 or 31 in the posterior cingulate cortex following a WGA-HRP injection into the caudal, intermediate or rostral portion of area TA. The present finding suggests that verbal and auditory memory impairment in patients with damage to the posterior cingulate cortex is largely due to damage to the CML and area 23b and not to the other posterior cingulate areas.

Direct projections from CA1 to the superior temporal sulcus in the monkey, revealed by single axon analysis

Anterograde tracer injections in the middle sector of CA1 in macaque monkeys demonstrate a direct projection to the fundus of the anterior superior temporal sulcus, in area IPa. Terminations are predominantly in layer 3. With regard to both terminal and arbor configuration, these hippocampal-cortical connections are morphologically similar to corticocortical connections to temporal association cortex. This report provides additional evidence of direct CA1 connections to particular multimodal cortical areas.