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Basic Organization of Projections from the Oval and Fusiform Nuclei of the Bed Nuclei of the Stria Terminalis in Adult Rat Brain

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Basic Organization of Projections from the Oval and Fusiform Nuclei of the Bed Nuclei of the Stria Terminalis in Adult Rat Brain THE JOURNAL OF COMPARATIVE NEUROLOGY 436:430–455 (2001) Basic Organization of Projections From the Oval and Fusiform Nuclei of the Bed Nuclei of the Stria Terminalis in Adult Rat Brain HONG-WEI DONG,1,2 GORICA D. PETROVICH,3 ALAN G. WATTS,1 AND LARRY W. SWANSON1* 1Neuroscience Program and Department of Biological Sciences, University of Southern California, Los Angeles, California 90089-2520 2Institute of Neuroscience, The Fourth Military Medical University, Xi’an, Shannxi 710032, China 3Department of Psychology, Johns Hopkins University, Baltimore, Maryland 21218 ABSTRACT The organization of axonal projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis (BST) was characterized with the Phaseolus vulgaris-leucoagglutinin (PHAL) anterograde tracing method in adult male rats. Within the BST, the oval nucleus (BSTov) projects very densely to the fusiform nucleus (BSTfu) and also innervates the caudal anterolateral area, anterodorsal area, rhomboid nucleus, and subcommissural zone. Outside the BST, its heaviest inputs are to the caudal substantia innominata and adjacent central amygdalar nucleus, retrorubral area, and lateral parabrachial nucleus. It generates moderate inputs to the caudal nucleus accumbens, parasubthalamic nucleus, and medial and ventrolateral divisions of the periaqueductal gray, and it sends a light input to the anterior parvicellular part of the hypothalamic paraventricular nucleus and nucleus of the solitary tract. The BSTfu displays a much more complex projection pattern. Within the BST, it densely innervates the anterodorsal area, dorsomedial nucleus, and caudal anterolateral area, and it moderately innervates the BSTov, subcommissural zone, and rhomboid nucleus. Outside the BST, the BSTfu provides dense inputs to the nucleus accumbens, caudal substantia innominata and central amygdalar nucleus, thalamic paraventricular nucleus, hypothalamic paraventricular and periventricular nuclei, hypothalamic dorsomedial nucleus, perifornical lateral hypothalamic area, and lateral tegmental nucleus. Moderately dense inputs are found in the parastrial, tuberal, dorsal raphe´, and para- brachial nuclei and in the retrorubral area, ventrolateral division of the periaqueductal gray, and pontine central gray. Light projections end in the olfactory tubercle, lateral septal nucleus, posterior basolateral amygdalar nucleus, supramammillary nucleus, and nucleus of the solitary tract. These and other results suggest that the BSTov and BSTfu are basal telencephalic parts of a circuit that coordinates autonomic, neuroendocrine, and ingestive behavioral responses during stress. J. Comp. Neurol. 436:430–455, 2001. © 2001 Wiley-Liss, Inc. Indexing terms: autonomic; central amygdalar nucleus; CRH; ingestive behavior; paraventricular nucleus of the hypothalamus; stress Many studies indicate that the bed nuclei of the stria bens (ventral striatum), substantia innominata (ventral terminalis (BST) play an important role in the coordina- pallidum), hypothalamus, midline thalamic nuclei, and tion of neuroendocrine, autonomic, and somatomotor re- sponses during behaviors associated with a definite affec- tive or emotional component (Casada and Dafny, 1991; Swanson, 1991; Gray et al., 1993; Dunn and Williams, Contract grant sponsor: National Institutes of Health; Contract grant 1995; Herman and Cullinan, 1997; Risold et al., 1997; number: 2R01NS16686; Contract grant number: NS29728; Contract grant number: NSKO401833. Watts, 2001). The BST receive massive, topographically *Correspondence to: Dr. L.W. Swanson, Hedco Neuroscience Building, organized inputs from most parts of the amygdala (Kret- Rm. 428, University of Southern California, Los Angeles, CA 90089-2520. tek and Price, 1978; Weller and Smith, 1982; Dong et al., E-mail: [email protected] 2001) and in turn project massively to the nucleus accum- Received 13 February 2001; Revised 3 April 2001; Accepted 15 May 2001 © 2001 WILEY-LISS, INC. BST PROJECTIONS 431 Abbreviations AAA anterior amygdalar area CUN cuneiform nucleus ac anterior commissure DMH dorsomedial nucleus hypothalamus ACB nucleus accumbens DMHa dorsomedial nucleus hypothalamus, anterior part aco anterior commissure, olfactory limb DMHp dorsomedial nucleus hypothalamus, posterior part act anterior commissure, temporal limb DMHv dorsomedial nucleus hypothalamus, ventral part ADP anterodorsal nucleus thalamus DMX dorsal motor nucleus vagus nerve AHA anterior hypothalamic area DR dorsal nucleus raphe´ AHN anterior hypothalamic nucleus DTN dorsal tegmental nucleus AHNa anterior hypothalamic nucleus, anterior part ENTl entorhinal area, lateral part AHNc anterior hypothalamic nucleus, central part EPv endopiriform nucleus, ventral part AHNd anterior hypothalamic nucleus, dorsal part EW Edinger-Westphal nucleus AHNp anterior hypothalamic nucleus, posterior part FF fields of Forel AMd anteromedial nucleus thalamus, dorsal part fi fimbria AP area postrema fr fasciculus retroflexus AQ cerebral aqueduct FS fundus of the striatum ARH arcuate nucleus hypothalamus fx columns of the fornix AVP anteroventral preoptic nucleus GP globus pallidus AVPV anteroventral periventricular nucleus hypothalamus GPl globus pallidus, lateral segment B Barrington’s nucleus GPm globus pallidus, medial segment BA bed nucleus accessory olfactory tract GR gracile nucleus BLAa basolateral amygdalar nucleus, anterior part GRN gigantocellular reticular nucleus BLAp basolateral amygdalar nucleus, posterior part IA intercalated nuclei amygdala BMAa basomedial amygdalar nucleus, anterior part IAM interanteromedial nucleus thalamus BMAp basomedial amygdalar nucleus, posterior part ic internal capsule BST bed nuclei of the stria terminalis IC inferior colliculus BSTad bed nuclei of the stria terminalis, anterior division, an- ICc inferior colliculus, central nucleus terodorsal area ICe inferior colliculus, external nucleus BSTal bed nuclei of the stria terminalis, anterior division, an- IF interfascicular nucleus terolateral area ILA infralimbic cortical area BSTav bed nuclei of the stria terminalis, anterior division, an- IMD intermediodorsal nucleus thalamus teroventral area INS insular cortical area BSTcc bed nuclei of the stria terminalis, anterior division, an- int internal capsule terodorsal area, central core isl islands of Calleja (olfactory tubercle) BSTd bed nuclei of the stria terminalis, posterior division, dor- IVn trochlear nerve sal nucleus KF Ko¨lliker-Fuse subnucleus (of PB) BSTdl bed nuclei of the stria terminalis, anterior division, dorso- LA lateral amygdalar nucleus lateral nucleus LC locus coeruleus BSTdm bed nuclei of the stria terminalis, anterior division, dorso- LDT laterodorsal tegmental nucleus medial nucleus LH lateral habenula BSTfu bed nuclei of the stria terminalis, anterior division, fusi- LHA lateral hypothalamic area form nucleus LM lateral mammillary nucleus BSTif bed nuclei of the stria terminalis, posterior division, inter- LPO lateral preoptic area fascicular nucleus LS lateral septal nucleus BSTju bed nuclei of the stria terminalis, anterior division, juxta- LSc lateral septal nucleus, caudal part capsular nucleus BSTmg bed nuclei of the stria terminalis, anterior division, mag- LSr lateral septal nucleus, rostral part nocellular nucleus LSr.vl.v. lateral septal nucleus, rostral part, ventrolateral zone, BSTov bed nuclei of the stria terminalis, anterior division, oval ventral region nucleus LSv lateral septal nucleus, ventral part BSTpr bed nuclei of the stria terminalis, posterior division, prin- LTN lateral tegmental nucleus cipal nucleus LV lateral ventricle BSTrh bed nuclei of the stria terminalis, anterior division, rhom- MA magnocellular preoptic nucleus boid nucleus MD mediodorsal nucleus thalamus BSTsc bed nuclei of the stria terminalis, anterior division, sub- MDc mediodorsal nucleus thalamus, central part commissural zone MDl mediodorsal nucleus thalamus, lateral part BSTse bed nuclei of the stria terminalis, posterior division, stria MDm mediodorsal nucleus thalamus, medial part extension MEAad medial nucleus amygdalar, anterodorsal part BSTsz bed nuclei of the stria terminalis, posterior division, cell- MEApd medial nucleus amygdalar, posterodorsal part sparse zone MEApv medial nucleus amygdalar, posteroventral part BSTtr bed nuclei of the stria terminalis, posterior division, MEPO median preoptic nucleus transverse nucleus MEV mesencephalic nucleus of the trigeminal BSTv bed nuclei of the stria terminalis, anterior division, ven- ml medial lemniscus tral nucleus mlf medial longitudinal fascicle CA1 field CA1, ammon’s horn MM medial mammillary nucleus CA2 field CA2, ammon’s horn moV motor root of the trigeminal nerve CA3 field CA3, ammon’s horn mp mammillary peduncle CEA central nucleus amygdala MPN medial preoptic nucleus CEAc central nucleus amygdala, capsular part MPO medial preoptic area CEAl central nucleus amygdala, lateral part MRN mesencephalic reticular nucleus CEAm central nucleus amygdala, medial part MS medial septal nucleus CLI central linear nucleus raphe´ mtt mammillothalamic tract CM central medial nucleus thalamus mtV mesencephalic tract of the trigeminal nerve COAa cortical nucleus amygdala, anterior part NDB nucleus of the diagonal band COApl cortical nucleus amygdala, posterior part, lateral zone NLOT nucleus of the lateral olfactory tract COApm cortical nucleus amygdala, posterior part, medial zone NTS nucleus of solitary tract COM commissural nucleus, periaqueductal gray NTSce nucleus of the solitary tract, central part CP caudoputamen NTSge nucleus of the solitary
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