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Cortical Afferents of the Perirhinal, Postrhinal, and Entorhinal Cortices of the Rat

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Cortical Afferents of the Perirhinal, Postrhinal, and Entorhinal Cortices of the Rat THE JOURNAL OF COMPARATIVE NEUROLOGY 398:179–205 (1998) Cortical Afferents of the Perirhinal, Postrhinal, and Entorhinal Cortices of the Rat REBECCA D. BURWELL1* AND DAVID G. AMARAL2 1Department of Psychology, Brown University, Box 1853, Providence, Rhode Island 02912 2Department of Psychiatry and Center for Neuroscience, The University of California, Davis, Davis, California 95616 ABSTRACT We have divided the cortical regions surrounding the rat hippocampus into three cytoarchitectonically discrete cortical regions, the perirhinal, the postrhinal, and the entorhi- nal cortices. These regions appear to be homologous to the monkey perirhinal, parahippocam- pal, and entorhinal cortices, respectively. The origin of cortical afferents to these regions is well-documented in the monkey but less is known about them in the rat. The present study investigated the origins of cortical input to the rat perirhinal (areas 35 and 36) and postrhinal cortices and the lateral and medial subdivisions of the entorhinal cortex (LEA and MEA) by placing injections of retrograde tracers at several locations within each region. For each experiment, the total numbers of retrogradely labeled cells (and cell densities) were estimated for 34 cortical regions. We found that the complement of cortical inputs differs for each of the five regions. Area 35 receives its heaviest input from entorhinal, piriform, and insular areas. Area 36 receives its heaviest projections from other temporal cortical regions such as ventral temporal association cortex. Area 36 also receives substantial input from insular and entorhinal areas. Whereas area 36 receives similar magnitudes of input from cortices subserving all sensory modalities, the heaviest projections to the postrhinal cortex originate in visual associational cortex and visuospatial areas such as the posterior parietal cortex. The cortical projections to the LEA are heavier than to the MEA and differ in origin. The LEA is primarily innervated by the perirhinal, insular, piriform, and postrhinal cortices. The MEA is primarily innervated by the piriform and postrhinal cortices, but also receives minor projections from retrosplenial, posterior parietal, and visual association areas. J. Comp. Neurol. 398:179–205, 1998. ௠ 1998 Wiley-Liss, Inc. Indexing terms: polysensory cortex; hippocampus; memory; spatial; retrograde Since the landmark studies of the famous amnesic performance on memory tasks (Hunt et al., 1994; Leonard patient H.M., research on the neural basis of memory has et al., 1995; Otto et al., 1991). Thus far, a specific memory focused on various structures in the medial temporal lobe function has not been identified for the parahippocampal (Scoville and Milner, 1957). Whereas earlier work empha- cortex, but studies in humans and monkeys suggest a sized the contribution of the hippocampus, and sometimes possible role in the processing of spatial information (Aquirre the amygdala, more recent emphasis has centered on the et al., 1996; Habib and Sirigu, 1987; Malkova and Mishkin, cortical regions that surround the hippocampus including 1997; Rolls and O’Mara, 1995). It is clear that the cortical the perirhinal, parahippocampal, and entorhinal cortices. regions surrounding the hippocampus are involved in memory The evidence now indicates that, in addition to providing functions, but their particular contributions and their the primary cortical input to the hippocampus, these functional interrelationships are not fully understood. regions make unique contributions to certain forms of memory. For example, damage limited to the perirhinal cortex is sufficient to cause memory deficits in visual object Grant sponsor: NIH; Grant number: NS 16980; Grant sponsor: NIMH; Grant number: F32-NS09247. recognition (Meunier et al., 1993; Ramus et al., 1994; Wiig *Correspondence to: Rebecca D. Burwell, Ph.D., Department of Psychol- et al., 1996) and visual discrimination learning (Buckley ogy, Brown University, Box 1853, Providence, RI 02912. and Gaffan, 1997; Myhrer and Wangen, 1996; Wiig et al., E-mail: [email protected] 1996). Selective lesions of the entorhinal cortex also affect Received 28 November 1997; Revised 2 April 1998; Accepted 14 April 1998 ௠ 1998 WILEY-LISS, INC. 180 R.D. BURWELL AND D.G. AMARAL The neuroanatomy of the monkey perirhinal, parahippo- between 300 and 400 g. The brains of 20 subjects, those campal, and entorhinal cortices has been extensively containing the 37 successful injection sites listed in Table examined (e.g., see Amaral et al., 1987; Jones and Powell, 1, were selected for more detailed analysis. Data on 1970; Suzuki and Amaral, 1994a,b; Van Hoesen and connections between the perirhinal, postrhinal, and ento- Pandya, 1972; Witter and Amaral, 1991; Witter et al., rhinal cortices from these cases have been previously 1989). Much less is known, however, about these regions in described (Burwell and Amaral, 1998). Prior to surgery, all the rat. Only a single study has comprehensively exam- subjects were housed individually or in pairs under stan- ined the afferents of the rat entorhinal cortex and that one dard vivarium conditions with ad libitum access to food largely ignored cortical afferents (Beckstead, 1978). There and water. Following surgery, subjects were housed indi- is also only a single comprehensive study of the cortical vidually. All methods involving the use of live subjects inputs to the rat perirhinal cortex (Deacon et al., 1983). were approved by the appropriate institutional animal Both of these studies, however, were based on areal care committee and conform to NIH guidelines. boundaries that have now undergone revision. We recently proposed that the perirhinal cortex in the rat be divided Surgery into two regions: a rostral region that bears cytoarchitec- One of two anesthesia protocols was used for each tonic and connectional similarities to the monkey perirhi- surgery; subjects were either injected with sodium pento- nal cortex, and a caudal portion, the postrhinal cortex, that barbital (n 5 17, Nembutal௡, Abbott Laboratories, North is similar connectionally to the monkey parahippocampal Chicago, IL, 50 mg/kg, i.p.) or brought to a surgical level cortex (Fig. 1; Burwell et al., 1995). The evidence now with halothane gas (n 5 29). A subject was then secured in indicates that the perirhinal and postrhinal cortices project a Kopf stereotaxic apparatus in the flat skull position. A preferentially to different portions of the entorhinal cortex hole was drilled into the skull above each intended injec- (Burwell and Amaral, 1998; Naber et al., 1997). These tion site and a small incision was made in the dura to findings highlight the importance of describing the topog- permit unobstructed penetration of the glass micropipette. raphy of the cortical afferents of these regions. The goal of After all injections were completed, the wound was su- the present series of studies was to provide a comprehen- tured and the animals were kept warm in their cages for sive and quantitative assessment of the cortical inputs to 1–2 hours before being returned to the colony. the entorhinal, perirhinal, and postrhinal cortices by using The retrograde tracers, Fast Blue or Diamidino Yellow modern tract tracing techniques and rigorous quantifica- (FB, DY, Dr. Illing, GmbH and Co., Gross Umstadt, tion of neuroanatomical material. Our goal was to conduct Germany), were injected at various locations within the studies in the rat that would provide data similar to those perirhinal, postrhinal, and entorhinal cortices by using that were previously acquired for the monkey brain (Insau- stereotaxic coordinates derived from Paxinos and Watson sti et al., 1987; Suzuki and Amaral, 1994a). These data (1986). For FB, approximately 150 nl of a 3% solution in would hopefully foster comparisons of the functional orga- distilled H O was injected. For DY, approximately 200 nl of nization of these memory-related brain regions in two 2 a 2% solution in distilled H2O was injected. All but one common animal models of human memory. subject received two retrograde tracer injections (FB and DY) and one anterograde tracer injection not relevant to MATERIALS AND METHODS the present study. The remaining subject, 108FG, received Subjects a single injection of 100 nl of a 2% solution of Fluoro-Gold (FG, Fluorochrome, Inc., Englewood, CO) in normal saline Subjects were 46 previously untreated male Sprague- (Schmued and Fallon, 1986). The tracers were pressure- Dawley rats (Harlan Laboratories, Houston, TX) weighing injected through glass micropipettes (tip diameters rang- Abbreviations ACAd dorsal anterior cingulate area ORBvl ventrolateral orbital area ACAv ventral anterior cingulate area PaSub parasubiculum AId dorsal agranular insular area PBS phosphate-buffered saline AIv ventral agranular insular area Par2 parietal cortex, area 2 AIp posterior agranular insular area Pir piriform cortex AUD primary auditory area PL prelimbic area AUDv ventral auditory area PR perirhinal cortex AUDp posterior auditory area POR postrhinal cortex CA1, CA2, PostSub postsubiculum CA3 CA fields of the hippocampus PTLp posterior parietal association areas DG dentate gyrus rs rhinal sulcus DY Diamidino yellow RSPd dorsal retrosplenial area EC entorhinal cortex RSPv ventral retrosplenial area FB Fast blue SSp primary somatosensory area FG Fluoro-Gold SSs supplementary somatosensory area GU gustatory area Te v ventral temporal association areas HPC hippocampus proper Te2 temporal cortex, area 2 ILA infralimbic area Te3 temporal cortex, area 3 LEA
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