1 Epilepsy Research Laboratory, AI Virtanen Institute for Molecular Sciences, University of Kuopio, PO Box 1627 and , 2 Department of Neurology, Kuopio University Hospital, PO Box 1777, FIN-70 211 Kuopio, Finland
Address correspondence to Dr Asla Pitkänen, AI Virtanen Institute for Molecular Sciences, University of Kuopio, PO Box 1627, FIN-70 211 Kuopio, Finland. Email: asla.pitkanen{at}uku.fi.
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Abstract |
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Introduction |
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Previous tract-tracing studies indicate that the lateral, basal and accessory basal nuclei of the amygdala innervate primarily the temporal end of the hippocampus, either monosynaptically or via the entorhinal cortex (Krettek and Price, 1977a; Pikkarainen et al., 1999
). The perirhinal and postrhinal cortices, in turn, project preferentially to the entorhinal subfields (Burwell et al., 1995
; Naber et al., 1997
; Burwell and Amaral, 1998
), which innervate the septal hippocampus and the subiculum in the rat (Ruth et al.1982
,1988
; Witter et al.1989
; Dolorfo and Amaral, 1998
). In addition, the perirhinal cortex innervates the septal subiculum/CA1 region monosynaptically (Deacon et al.1983
; Kosel et al.1983
; Romanski and LeDoux, 1993
; McIntyre et al.1996
; Naber et al.1999
; Shi and Cassell, 1999
). In the rat, the perirhinal and postrhinal cortices are heavily interconnected with each other as well as with the entorhinal cortex (Burwell et al.1995
; Naber et al.1997
; Burwell and Amaral, 1998
). Therefore, monosynaptic projections from the amygdaloid complex to the perirhinal and postrhinal cortices provide a pathway via which the amygdala could modulate the neuronal activity in the septal hippocampus polysynaptically. Such projections also provide a route via which the amygdala could innervate these two cortical components of the medial temporal lobe memory system monosynaptically in parallel.
Projections from the amygdala to the perirhinal cortex in the rat have been investigated in previous tract-tracing studies (Krettek and Price, 1977a,b
; Deacon et al.1983
; McDonald and Jackson, 1987
; Arnault and Roger, 1990
; Petrovich et al.1996
). In most of these reports, however, tracer injections were not limited to one subdivision of the amygdala (anterograde tracers) or a specific region of the perirhinal cortex (retrograde tracers), and therefore many of the details of these connections are lacking. Further, to our knowledge, the projections from the amygdala to the rat postrhinal cortex have not been investigated in detail. Here, we investigated the distribution and topography of projections from the amygdala to the perirhinal and postrhinal cortices in rat by placing small injections of the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHA-L) into different divisions of the lateral, basal and accessory basal nuclei of the amygdala. The data indicate that these projections are abundant and highly topographically organized.
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Materials and Methods |
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Male Wistar rats (National Laboratory Animal Center, Kuopio, Finland) weighing 275350 g were used. The experiments were approved by the provincial government of Kuopio, Finland. All animal procedures were conducted in accordance with the guidelines of the European Community Council directives 86/609/EEC.
Rats were anesthetized i.p. (4 ml/kg) with a mixture of sodium pentobarbital (9.7 mg/ml), chloral hydrate (10 mg/ml), magnesium sulfate (21.2 mg/ml), propylene glycol (40%) and ethanol (10%). The anterograde tracer PHA-L (2.5% in 0.1 M sodium phosphate buffer, pH 7.4; #L-1100, Vector, Burlingame, CA) was injected iontophoretically (positive-pulsed 4 µA current, 7 s on and 7 s off for 810 min) into the lateral nucleus (n = 20) (Pikkarainen et al.1999), basal nucleus (n = 16) (Savander et al.1995
) or accessory basal nucleus (n = 17) (Savander et al.1996
; Pikkarainen et al.1999
) of the left amygdala. A detailed description of the surgical and injection procedures as well as of the processing and storing of the sections has been described previously (Pitkänen et al.1995
; Pikkarainen et al.1999
).
To identify PHA-L-immunoreactive fibers, a one-in-five series of sections was processed according to the immunohistochemical staining method described previously (Gerfen and Sawchenko, 1984). The primary antibody used was rabbit anti-PHA-L (dilution 1:8,000; #B275, DAKO, Glostrup, Denmark or #AD1818, Chemicon, Temecula, CA), and the PHA-L was visualized by incubating the sections in a solution containing 0.05% diaminobenzidine (#34001, Pierce, Rockford, IL) and 0.04% hydrogen peroxide in 0.02 M KPBS (pH 7.4). For a detailed description of the immunohistochemical staining procedure, see Savander et al. (Savander et al.1995
). An adjacent series of sections was stained with thionin to identify the borders of the various amygdaloid nuclei and regions of the perirhinal and postrhinal cortices.
Analysis of Sections
The sections were analyzed microscopically under brightfield and darkfield illumination. PHA-L-filled cell bodies in the injection site were plotted with a computer-aided digitizing system (Minnesota Datametrics, St Paul, MN) from every fifth section (one-in-five series, 30 µm thick). An adjacent thionin-stained section was superimposed on top of the computer-generated plot under a stereomicroscope equipped with a drawing tube, and the outlines of the amygdaloid nuclei were drawn on each plot using a camera lucida.
PHA-L-labeled fibers were considered to constitute a terminal plexus if they were thin and branching, and had varicosities (e.g. the terminal plexus in layers IV of area 35 in Fig. 4C). If the labeled fibers were thick and straight, with few or no varicosities, they were considered to be passing fibers (e.g. fibers passing through layer VI of area 35 in Fig. 4C,D
). The density of PHA-L-labeled terminals was determined based on visual assessment and assigned to one of four density grades of terminal labeling: very light or passing fibers (e.g. the sparse straight fibers in layer VI of area 36 in Fig. 4B
, which appear nonvaricose under a higher magnification), light (e.g. the individual criss-crossing fibers in layer I of area 36 in Fig. 4C
, which have a large number of varicosities under a higher magnification), moderate (e.g. the plexus of terminals on dark background in layer III of area 35 in Fig. 4C
) or heavy (e.g. the dense plexus of fibers in the deep portion of layer I of area 35 in Fig. 4C
, which entirely covers the background).
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Brightfield photomicrographs were taken with a Nikon Multiphot 6 x 9 cm system (Nikon, Tokyo, Japan). Darkfield photomicrographs were taken with a Nikon Microphot-FXA camera system (Nikon, Tokyo, Japan). The outlines of cytoarchitectonic boundaries and layers of the perirhinal and postrhinal cortices were drawn from thionin-stained sections with the aid of a stereomicroscope equipped with a drawing tube. Thereafter, the darkfield photomicrographs were scanned using a UMAX scanner linked to a Power Macintosh computer and the background and dust spots were removed by painting with Adobe Photoshop 4.0 software. Finally, the scanned outlines were redrawn using Canvas 3.5 software and superimposed on the scanned photomicrographs.
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Results |
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The Amygdaloid Complex
In the present study, we used a slight modification of the nomenclature of Price and co-workers (Price et al.1987) for the rat amygdaloid complex [for modifications, see Pitkänen et al. (Pitkänen et al.1997
,2000
)]. The deep nuclei of the amygdala consist of the lateral nucleus (dorsolateral, ventrolateral and medial divisions), the basal nucleus (magnocellular, intermediate and parvicellular divisions) and the accessory basal nucleus (magnocellular and parvicellular divisions) (Fig. 1
).
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The cytoarchitectonic borders of the perirhinal and postrhinal cortices were defined according to Burwell and co-workers (Burwell et al.1995; Burwell and Amaral, 1998
). Briefly, the perirhinal cortex is bordered rostrally by the insular cortex and caudally by the postrhinal cortex. The perirhinal cortex can be partitioned into areas 35 and 36 (Fig. 2
). Area 35 is narrower, and occupies the ventral bank and the fundus of the rhinal sulcus. Area 36 is dorsal to area 35 and occupies the dorsal bank of the rhinal sulcus. The postrhinal cortex is caudal to the perirhinal cortex and dorsal to the rhinal sulcus (Fig. 2
).
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We analyzed 53 PHA-L injections and a large majority of the tracer-filled cells were localized within one subdivision of the lateral (n =20), basal (n = 16) or accessory basal (n = 17) nucleus (Fig. 1, Tables 13
) (Savander et al.1995
,1996
; Pikkarainen et al., 1999
). Typically, the injection site extended through 35 sections (section thickness 30 µm, one-in-five series). The distribution and density of terminal labeling in the perirhinal and postrhinal cortices was more dependent on the location of the injection within the amygdala rather than on the number of labeled neurons at the injection site. In occasional cases, we found a few PHA-L-positive cells in the surrounding amygdaloid nuclei or cortical areas (e.g. periamygdaloid cortex or piriform cortex), or along the injection tract within the striatum. When the appearance of terminal labeling in the perirhinal and postrhinal cortices was compared with that in pure amygdaloid injections, we concluded that such contamination of injection sites provided only a minor contribution, if any, to the projection pattern. Next, the projection patterns in the perirhinal and postrhinal cortices from each deep amygdaloid nucleus or nuclear subdivision are described.
Projections to the Perirhinal Cortex: Area 35
Lateral Nucleus
The dorsolateral and medial divisions of the lateral nucleus originated the heaviest projections from the amygdala to area 35 (Figs 35, Table 1
). The dorsolateral division heavily innervated almost the entire rostrocaudal extent of area 35, whereas the projection from the medial division was limited mostly to its caudal aspect. That is, caudal to the level of 4.0 from bregma (Paxinos and Watson, 1986
) the density of terminal labeling increased rapidly from very light to moderate-to-heavy (e.g. Fig. 5C,D
). Typically, labeled terminals covered the entire dorsoventral extent of the area. Analysis of the laminar distribution of labeling indicated that the projection from the dorsolateral division terminated most heavily in the deep portion of layer I, in layer II and in the superficial portion of layer III (Fig. 4
, Table 1
). The medial division, in turn, innervated most heavily layers IV (Fig. 5D,E
, Table 1
).
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Projections from the ventrolateral division were substantially lighter than those from the dorsolateral and medial divisions (Fig. 3, Table 1
) and they terminated primarily in the deep portion of the layer I, layers II and III, and layer V of caudal area 35 (Table 1
).
Basal Nucleus
The magnocellular division of the basal nucleus provided substantial projections to the rostral one-third of area 35 (Figs 3 and 6B,C). Within this region, the projection was heavier rostrally than caudally and extended throughout the entire dorsoventral extent of area 35. The highest density of terminal labeling was located in layers V and VI, whereas layers II and III contained only light labeling (Fig. 6BD
, Table 2
). The projection to area 35 formed a continuum with the projection terminating in the rostrally located insular cortex.
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Accessory Basal Nucleus
The accessory basal nucleus gave origin to substantial projections to area 35, which were, however, less prominent than those from the lateral nucleus (Figs 3 and 7, Table 3
). The projections from the parvicellular division were moderate in density and terminated throughout the dorsoventral extent of layer V of caudal area 35 (Figs 3 and 7
, Table 3
). Rostrally, the labeling was lighter and innervated only the ventral aspect of area 35 (Fig. 3
).
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Projections to the Perirhinal Cortex: Area 36
Lateral Nucleus
The projection from the lateral nucleus to area 36 was substantially lighter than that to area 35 (Figs 35, Table 1
). The dorsolateral division innervated mainly the caudal two-thirds of ventral area 36 (Figs 3 and 4
). Projections terminated in layer I, whereas layers IIVI contained only a few terminals intermingled with passing fibers. In the more dorsal aspect of area 36, the light projection terminated almost exclusively in layer I (Fig. 4BD
).
The ventrolateral and medial divisions projected lightly to area 36 (Figs 3 and 5, Table 1
). The ventrolateral division mainly innervated layer V of the ventral extreme of area 36 (Fig. 3
). The medial division, particularly its rostral portion, projected to layers IVI of the caudal two-thirds of the most ventral extreme of area 36 (Figs 3 and 5
, Table 1
). Only the projection to layers I and V reached the more dorsal aspect of area 36 (Fig. 5C,D
).
Basal Nucleus
The projection from the magnocellular division to area 36 was even heavier than that to area 35 (Figs 3 and 6, Table 2
). The projection terminated mainly in layers V and VI of the rostral portion of area 36 (Figs 3 and 6B,C
, Table 2
). As in area 35, the projection to area 36 extended throughout its dorsoventral extent (Figs 3 and 6
).
Projections from the intermediate and parvicellular divisions to area 36 were less prominent than projections from the magnocellular division (Fig. 3, Table 2
). The intermediate division projected lightly to layers V and VI, whereas the parvicellular division provided a light projection to layer V of the rostral portion of area 36.
Accessory Basal Nucleus
The magnocellular division originated a light-to-moderate projection mainly to layers IIII of the rostroventral aspect of the area 36 (Fig. 3, Table 3
). The parvicellular division, in turn, provided a light projection to layers IV of the most ventral aspect of area 36 (Figs 3 and 7
, Table 3
).
Projections to the Postrhinal Cortex
Lateral Nucleus
The dorsolateral and medial divisions provided heavy topographically organized projections to the postrhinal cortex (Figs 3, 4F,G and 5F,G, Table 1
). The highest density of terminal labeling was observed in layers IIII of the rostroventral aspect of the postrhinal cortex. The dorsoventral and laminar distribution of labeled fibers depended, however, on the location of the injection in the dorsolateral and medial divisions. First, the rostral dorsolateral division projected mainly to layer I of the ventral postrhinal cortex (Fig. 3
). The caudal portion projected to layers IIII of the ventral, as well as to layer I of the more dorsal aspect of the postrhinal cortex (Fig. 4F,G
). Secondly, the rostral portion of the medial division projected lightly to layers IV of the more dorsal aspect of the postrhinal cortex (Fig. 5F
).
The ventrolateral division originated the weakest projection from the lateral nucleus to the postrhinal cortex (Fig. 3, Table 1
). Light terminal labeling innervated layers IV of the rostral two-thirds of the most ventral postrhinal cortex.
Basal Nucleus
The basal nucleus did not project to the postrhinal cortex. In some cases, there were occasional straight nonvaricose fibers that resembled fibers en passage in the deep layers of the ventral aspect of the postrhinal cortex (Table 2).
Accessory Basal Nucleus
The accessory basal nucleus also provided substantial input to the postrhinal cortex, even though the projections were lighter than those from the lateral nucleus (Figs 3 and 7, Table 3
). Typically, the accessory basal nucleus innervated layers IIII of the rostroventral aspect of the postrhinal cortex. Projections arising in the parvicellular division were light-to-moderate in density (Fig. 7
), whereas the magnocellular division originated only light projections.
Contralateral Projections
There were no contralateral projections from the lateral and basal nuclei to the perirhinal or postrhinal cortices. Injections into the accessory basal nucleus occasionally gave rise to some light labeling in contralateral area 35 (in 7/17 cases). In some of the cases, labeling was observed mainly in layer I, whereas the other cases contained labeling in layers IVI.
Course of Fibers from the Deep Amygdaloid Nuclei to the Perirhinal and Postrhinal Cortices
Projections originating in the lateral nucleus traveled first through the nucleus, then the external capsule and thereafter the angular bundle, before arriving in the deep layers of the perirhinal and postrhinal cortices.
PHA-L-filled fibers from the magnocellular and intermediate divisions of the basal nucleus traveled through the lateral portion of the parvicellular division. After leaving the basal nucleus, these fibers, as well as the fibers from the parvicellular division of the basal nucleus, traversed the external capsule and entered the perirhinal and postrhinal cortices through their deep layers. Some of these fibers appeared to travel first through the lateral nucleus before entering the external capsule.
Tracer-filled fibers from the accessory basal nucleus traveled first through the parvicellular and intermediate divisions of the basal nucleus, then joined at the external capsule and/or the angular bundle to enter the deep layers of the perirhinal and postrhinal cortices. Some labeled fibers seemed to traverse the external capsule, the endopiriform nucleus, and the deep layers of the piriform and entorhinal cortices before entering the perirhinal cortex.
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Discussion |
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Several previous studies report projections from the lateral (Krettek and Price, 1977a,b
; Ottersen, 1982
; Deacon et al.1983
; McDonald and Jackson, 1987
; Arnault and Roger, 1990
), basal (Krettek and Price, 1977b
; McDonald and Jackson, 1987
) or accessory basal (McDonald and Jackson, 1987
; Petrovich et al.1996
) nuclei of the amygdala to the perirhinal cortex in rat. Little, however, is known regarding the projections from the amygdala to the postrhinal cortex (Krettek and Price, 1977a
; Deacon et al.1983
).
Consistent with previous observations, the heaviest amygdaloid projections to the perirhinal cortex originate in the lateral nucleus (McDonald and Jackson, 1987). Topographic analysis of these projections indicates that they terminate in layers IV throughout the dorsoventral extent of area 35, whereas projections to area 36 are relatively meager and terminate only in its narrow ventral-most aspect. Like the lateral nucleus, the accessory basal nucleus innervates mainly area 35, area 36 being only lightly innervated. The density of this projection, however, is lighter than that from the lateral nucleus but heavier than that from the basal nucleus. Previously, Krettek and Price (Krettek and Price, 1977b
) suggested that the projections from the basal nucleus to the perirhinal cortex terminate mainly in layers I and VI. Our data reveal that the main projections from the basal nucleus terminate in layer V of rostral area 35 and in layers V and VI of rostral area 36, and that there are only occasional PHA-L-labeled fibers in the superficial layers. Finally, the present findings indicate that the lateral and accessory basal nuclei provide substantial projections to layers IIII of the rostroventral postrhinal cortex.
The most important new finding of the present study is that the distribution and density of projections are highly dependent on the subdivisional location of the PHA-L injection within the amygdaloid nuclei. For example, the medial division of the lateral nucleus projects heavily to layers IV of caudal area 35 and to layers IIII of the rostroventral postrhinal cortex, whereas the dorsolateral division also innervates area 35 more rostrally as well as layer I of ventral area 36. Projections from the ventrolateral division of the lateral nucleus to the perirhinal and postrhinal cortices are meager. Within the basal nucleus, the most substantial projections originate in the magnocellular division and terminate in the rostral aspects of areas 35 and 36. The caudomedial portion of the parvicellular division provides light projections to the caudal two-thirds of the perirhinal cortex. Finally, within the accessory basal nucleus, most of the projections originate in the parvicellular division and terminate in layer V of caudal area 35. Lighter projections from the magnocellular division terminate in layers IIII of area 35 as well as in layers IIII of the adjacent rostroventral area 36.
Organization of Projections from the Amygdala to the Perirhinal and Postrhinal Cortices
The analysis of projections from the lateral, basal and accessory basal nuclei to the perirhinal and postrhinal cortices reveals four major principles in the organization of these pathways. First, only selective nuclei or nuclear divisions give rise to these projections. For example, the most prominent projections originate in the medial and dorsolateral divisions of the lateral nucleus, in the magnocellular division of the basal nucleus and in the parvicellular division of the accessory basal nucleus. These observations suggest that, like the projections from the amygdala to the other functional systems (e.g. from the central nucleus to the brain stem autonomic centers), the projections to the medial temporal cortex have selective output regions in the amygdaloid complex.
Secondly, many of the nuclei or nuclear divisions provide substantial parallel inputs to more than one area within the perirhinal and postrhinal cortices. For example, the medial division of the lateral nucleus substantially innervates both caudal area 35 and caudoventral area 36 as well as the rostroventral postrhinal cortex. The magnocellular division of the basal nucleus innervates both rostral area 35 as well as rostral area 36. Perhaps the most point-to-point organized projections originate in the magnocellular and parvicellular divisions of the accessory basal nucleus, which terminate in rostral area 35 and caudal area 35, respectively. It remains to be studied whether the parallel projections from the lateral and basal nuclei to the different cortical areas originate in the same or different neurons.
Both areas 35 and 36, as well as the rostroventral postrhinal cortex, receive substantial inputs from the amygdala. There are, however, clear rostrocaudal, dorsoventral and laminar topographies in the organization of these projections. For example, the rostral perirhinal cortex is innervated only by the magnocellular division of the basal nucleus and the magnocellular division of the accessory basal nucleus. The caudal aspects of the perirhinal cortex receive inputs from the medial and dorsolateral divisions of the lateral nucleus as well as from the parvicellular division of the accessory basal nucleus. The dorsoventral topography is the most distinct in caudal area 36 and the postrhinal cortex. The dorsal aspects of these regions do not receive any substantial inputs from the amygdala whereas their ventral aspects are heavily innervated by the dorsoventral and medial divisions of the lateral nucleus. Analysis of the laminar topography indicates that in area 35, particularly caudally, many of the projections terminate throughout layers IVI. In caudal area 36 and in the postrhinal cortex, however, the distribution of terminal labeling is limited to the superficial layers.
Some regions of the perirhinal and postrhinal cortices converge information from more than one nucleus or nuclear subdivision. For example, layer V of caudal area 35 receives substantial inputs from the medial division of the lateral nucleus as well as the parvicellular division of the accessory basal nucleus. Another example is layers I and II of the postrhinal cortex, which converge information from the dorsolateral and medial divisions of the lateral nucleus. In general, however, the perirhinal cortex converges information from all deep nuclei, whereas the postrhinal cortex is innervated by only the lateral nucleus.
Functional Aspects
The present and our previous study (Pikkarainen et al.1999) indicate that the deep amygdaloid nuclei provide substantial parallel inputs to different components of the parahippocampal hippocampal network [for a definition of the parahippocampal and hippocampal areas, see Scharfman et al. (Scharfman et al.2000
)]. For example, the lateral nucleus heavily innervates the parahippocampal region, including the perirhinal, postrhinal and entorhinal cortices, and the parasubiculum. The basal nucleus is the major source of projections from the amygdala to the hippocampus. These pathways innervate the temporal end of the CA3 and the CA1 subfields, and the temporal subiculum. The accessory basal nucleus, in turn, provides substantial inputs both to the parahippocampal areas, including the perirhinal and entorhinal cortices and the parasubiculum, and to the hippocampus, including the CA1 subfield. The functional significance of the parallel innervation of the different levels of the parahippocampalhippocampal system by the amygdala remains to be studied.
Area 35, ventral area 36 and the rostroventral postrhinal cortex receive the heaviest inputs from the amygdala. These cortical regions project heavily to the lateral entorhinal cortex (Burwell et al.1995; Naber et al.1997
; Burwell and Amaral, 1998
), which in turn projects to the septal and midseptotemporal levels of the hippocampus (Ruth et al.1982
,1988
; Witter et al.1989
; Dolorfo and Amaral, 1998
). Because the monosynaptic inputs from the amygdala to the hippocampus are directed to its temporal aspect (Krettek and Price, 1977a
; Pikkarainen et al.1999
), projections from the amygdala to the perirhinal and postrhinal cortices provide a route via which the amygdala can also modulate the more septal aspects of the hippocampus.
Some of the interconnections between the amygdala and the perirhinal and postrhinal cortices appear to be reciprocal (Ottersen, 1982; McDonald and Jackson, 1987
; Romanski and LeDoux, 1993
; Shi and Cassell, 1999
). A retrograde study by Shi and Cassell (Shi and Cassell, 1999
) demonstrated that the lateral nucleus receives substantial inputs from layers IIVI of the dorsal bank of the perirhinal cortex (corresponding area 36) and the fundus of the rhinal sulcus (corresponding area 35), as well as from the superficial layers of the postrhinal cortex [levels 7.6 and 8.0 in figs 18 and 19 of Shi and Cassell (Shi and Cassell, 1999
)]. We have demonstrated, however, that these regions are innervated by the lateral nucleus, even though the projection from the lateral nucleus does not extend as dorsally in area 36 as the projection from this region to the lateral nucleus. The accessory basal nucleus is also reciprocally connected with areas 35 and 36, even though the overall density of projections is lighter than that of the lateral nucleus (Shi and Cassell, 1999
). Projections from the perirhinal cortex to the basal nucleus are, however, substantially heavier than the projections from the basal nucleus to the perirhinal cortex, as we (present study) and others (Shi and Cassell, 1999
) have shown.
How similar is the organization of projections from the amygdala to the perirhinal and postrhinal cortices in rat compared with that in nonhuman primates? If we accept the recently proposed view that the perirhinal cortex (areas 35 and 36) and the postrhinal cortex in rat (Burwell et al.1995) correspond to the perirhinal cortex (areas 35 and 36) and the parahippocampal cortex (areas TH and TF) in the monkey [see the discussion in Burwell (Burwell, 2000
)], respectively, there are both similarities and differences in the organization of projections from the amygdala to these regions. First, as in the rat, the monkey lateral and accessory basal nuclei also provide substantial projections to the perirhinal cortex. In the monkey, however, the intermediate and parvicellular divisions of the basal nucleus also project to the perirhinal cortex (Stefanacci et al.1996
). Further, in rats these projections terminate mainly in area 35 and in a narrow ventral-most strip of the dorsally adjacent area 36. In contrast, in monkeys, the amygdala appears to innervate mainly area 36 (Stefanacci et al.1996
). Secondly, analysis of retrograde-tracer injections indicates that the major source of projections from the amygdala to the parahippocampal cortex in the monkey is the magnocellular (and intermediate) division of the basal nucleus (Stefanacci et al.1996
). In the rat, the postrhinal cortex is innervated mainly by the lateral and accessory basal nuclei.
Recent studies indicate that one of the major functions of the amygdala is to enhance memory formation for emotionally arousing events in rats, nonhuman primates and humans (Ikegaya et al., 1994, 1995
, 1996
; Packard et al.1994
; Roozendaal and McGaugh, 1997
; Cahill and McGaugh, 1998
; Packard and Teather, 1998
; ,Hamann et al.1999
; McGaugh, 2000
). The topographically organized projections from the amygdala to the hippocampal formation and parahippocampal area [see also Pikkarainen et al. (Pikkarainen et al., 1999
)] provide candidate pathways in which such functions can be processed. Another function in which the amygdaloid projections to the perirhinal and postrhinal cortices might have an important role is the spread of seizure activity from the amygdala to the hippocampus and surrounding cortex (Gloor, 1992
).
Taken together, the present data indicate that the lateral, basal and accessory basal nuclei of the rat amygdala provide substantial topographically organized projections to the perirhinal and postrhinal cortices. These connections provide candidate pathways via which the amygdala can modulate memory formation for emotionally arousing stimuli as well as spread seizure activity from the amygdala to the parahippocampal regions in temporal lobe epilepsy.
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Acknowledgments |
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Abbreviations |
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AB accessory basal nucleus |
ABmc accessory basal nucleus, magnocellular division |
ABpc accessory basal nucleus, parvicellular division |
AE entorhinal cortex, amygdaloentorhinal subfield |
AHAl amygdalohippocampal area, lateral division |
AHAm amygdalohippocampal area, medial division |
area 35 area 35 of the perirhinal cortex |
area 36 area 36 of the perirhinal cortex |
BAOT bed nucleus of the accessory olfactory tract |
Bi basal nucleus, intermediate division |
Bmc basal nucleus, magnocellular division |
Bpc basal nucleus, parvicellular division |
c central nucleus, capsular division |
CA1 CA1 field of the hippocampus |
CA3 CA3 field of the hippocampus |
CE entorhinal cortex, caudal entorhinal subfield |
CEi central nucleus, intermediate division |
CEl central nucleus, lateral division |
COa anterior cortical nucleus |
COp posterior cortical nucleus |
DIE entorhinal cortex, dorsal intermediate entorhinal subfield |
DLE entorhinal cortex, dorsal lateral entorhinal subfield |
I intercalated nucleus |
Ldl lateral nucleus, dorsolateral division |
Lm lateral nucleus, medial division |
Lvl lateral nucleus, ventrolateral division |
m central nucleus, medial division |
Mc medial nucleus, caudal division |
Mcd medial nucleus, dorsal portion of the central division |
Mcv medial nucleus, ventral portion of the central division |
ME entorhinal cortex, medial entorhinal subfield |
Mr medial nucleus, rostral division |
PAC periamygdaloid cortex |
PACm periamygdaloid cortex, medial division |
paraSUB parasubiculum |
POR postrhinal cortex |
SUB subiculum |
TF area TF of the parahippocampal cortex |
TH area TH of the parahippocampal cortex |
VIE entorhinal cortex, ventral intermediate entorhinal subfield |
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References |
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