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Connections of Some Auditory-Responsive Posterior Thalamic Nuclei Putatively Involved in Activation of the Hypothalamo

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THE JOURNAL OF COMPARATIVE NEUROLOGY 423:474–491 (2000) Connections of Some Auditory-Responsive Posterior Thalamic Nuclei Putatively Involved in Activation of the Hypothalamo– Pituitary–Adrenocortical Axis in Response to Audiogenic Stress in Rats: An Anterograde and Retrograde Tract Tracing Study Combined With Fos Expression SERGE CAMPEAU* AND STANLEY J. WATSON, JR. Mental Health Research Institute, The University of Michigan, Ann Arbor, Michigan 48109-0720 ABSTRACT Prior studies in our laboratory demonstrated that part of the thalamus is necessary for activating the hypothalamo–pituitary–adrenocortical (HPA) axis in response to audiogenic stress in rats. The present studies were designed to determine how the auditory-responsive thalamic nuclei might activate the HPA axis. Both retrograde [Fluoro-Gold (FG)] and anterograde [Pha- soleus vulgaris-leucoagglutinin (PHA-L) and biotinylated dextran amines (BDA)] tracers were employed to study the putative connectivity between the thalamus and the medial parvocellular region of the hypothalamic paraventricular nucleus (PAmp). In addition, rats receiving FG in the PAmp were subjected to audiogenic stress, and the distribution of both FG and the protein product of the immediate-early gene c-fos, Fos, were determined by double immunohistochem- istry, to help assess putative functional links between the auditory-responsive thalamic nuclei and PAmp. The results of PAmp FG placement indicated retrogradely labeled cells in several areas, including the bed nucleus of the stria terminalis, hypothalamic regions, the supramam- millary nucleus, some thalamic regions, and importantly, a few multisensory nuclei of the thalamus, including the parvicellular division of the subparafascicular and posterior intralami- nar nuclei. Injections of the tracers PHA-L or BDA into these auditory-responsive posterior thalamic nuclei provided further evidence of projections to the PAmp. In addition, several forebrain areas were observed to receive moderate to heavy innervation. These areas included most of the regions described above, which, in turn, project to the PAmp. Because cells in the multisensory thalamic nuclei, hypothalamic, and forebrain areas were double labeled with FG and Fos, the results suggest that either direct projections from the thalamus to PAmp neurons, or indirect projections from the thalamus to stress-responsive forebrain areas projecting to the PAmp, might mediate activation of the HPA axis by audiogenic stress. J. Comp. Neurol. 423: 474–491, 2000. © 2000 Wiley-Liss, Inc. Indexing terms: subparafascicular; intralaminar; preoptic; hypothalamus; noise; immunohistochemistry One of the defining characteristics of stress involves the secretion of glucocorticoids from the hypothalamo- Grant sponsor: NIMH; Grant number: MH-42251; Grant sponsor: Med- pituitary-adrenocortical axis (HPA) (Levine and Ursin, ical Research Council of Canada. 1991; Ursin and Olff, 1993; Akil and Morano, 1995; *Correspondence to: Serge Campeau, Ph.D., the Department of Psychol- ogy, P.O. Box 345, University of Colorado, Boulder, CO 80309-0345. Toates, 1995; Akil and Morano, 1996; Yehuda, 1997). The E-mail: [email protected] release of glucocorticoids in response to stressful stimuli Received 2 July 1999; Revised 18 February 2000; Accepted 28 March is, in most instances, ultimately controlled by neurons of 2000 © 2000 WILEY-LISS, INC. AUDITORY-RESPONSIVE THALAMIC AFFERENTS 475 the medial parvocellular region of the paraventricular remains largely speculative (Cullinan et al., 1996; Her- nucleus of the hypothalamus (PAmp), which contain man et al., 1996; Sawchenko et al., 1996; Herman and corticotropin-releasing factors, such as corticotropin- Cullinan, 1997; Li and Sawchenko, 1998). releasing hormone (CRH), arginine vasopressin (AVP), Recently, we observed that audiogenic stress elicits the and others (Antoni, 1986; Swanson et al., 1988; release of corticosterone, which is associated with a dis- Sawchenko, 1991). The release of corticotropin releasing- tinct pattern of brain activity in rats, as evidenced by the factors at the level of the external zone of the median induction of the immediate-early gene c-fos (Campeau and eminence, in the portal blood system, initiates the produc- Watson, 1997). Exposure of rats to intense white noise (90 tion and release of anterior pituitary adrenocorticotropin and 105 dBA for 30 minutes) produced significant c-fos hormone (ACTH) in the general circulation, which in turn mRNA induction in a handful of forebrain areas (the ven- induces the production and release of adrenal glucocorti- trolateral septum, septohypothalamic nucleus, anteroven- coids (corticosterone in rats). tral and anteromedial divisions of the bed nucleus of the It has thus been postulated that the paraventricular nucleus of the hypothalamus provides the central “final stria terminalis, lateral preoptic area, medial preoptic nu- common relay,” ultimately involved in the release of glu- cleus, and ventral dentate gyrus), compared with rats cocorticoids. However, there are very few instances in exposed to lower, nonstressful noise levels. Most of these which the control of the HPA axis has been ascribed to a audiogenic stress-responsive forebrain structures have di- specific set of anatomical afferents to the PAmp. One of rect projections to regions of the paraventricular hypotha- these provides hypophysiotropic afferents from the cat- lamic nucleus (Tribollet and Dreifuss, 1981; Sawchenko echolaminergic cell groups of the nucleus of the solitary and Swanson, 1983; Simerly and Swanson, 1988; Bitten- tract and ventrolateral medulla involved in HPA activa- court et al., 1991; Cullinan et al., 1993, 1996; Larsen et al., tion by an immune challenge (Li et al., 1996). Exactly how 1994; Moga and Saper, 1994; Herman et al., 1996; Li and most other stressors control the activity of the HPA axis Sawchenko, 1998). Abbreviations 3v third ventricle MnPO median preoptic nucleus ac anterior commissure MPA medial preoptic area aca anterior part of the anterior commissure MPO medial preoptic nucleus AcbC accumbens nucleus, core mp mammillary peduncle AcbSh accumbens nucleus, shell MS medial septal nucleus ACe central nucleus of the amygdala mt mammillothalamic tract ACo anterior cortical amygdaloid nucleus mtg mammillotegmental tract ADP anterodorsal preoptic nucleus MTu medial tuberal nucleus AH anterior hypothalamic opt optic tract Aq aqueduct of Sylvius ox optic chiasm ar acoustic radiation PAG periaqueductal gray Arc arcuate nucleus PAap paraventricular nucleus of the hypothalamus, anterior AStr amygdalostriatal transition area nucleus BL basolateral nucleus of the amygdala PAlm paraventricular nucleus of the hypothalamus, lateral BLA anterior basolateral nucleus of the amygdala magnocellular division BLV ventral basolateral nucleus of the amygdala PAmp paraventricular nucleus of the hypothalamus, medial par- BM basomedial nucleus of the amygdala vocellular division BMA anterior basomedial nucleus of the amygdala PBP pigmented parabrachial nucleus BST bed nucleus of the stria terminalis Pe periventricular nucleus of the hypothalamus BSTIA bed nucleus of the stria terminalis, intraamygdaloid divi- PeF perifornical nucleus sion PIL posterior intralaminar nucleus cp cerebral peduncle PP peripeduncular nucleus CPu caudate-putamen PH posterior hypothalamic area csc commissure of the superior colliculus pm principal mammillary tract cst commissure of the stria terminalis PoT posterior thalamic nucleus DLG dorsal lateral geniculate nucleus PS parastrial nucleus DMH dorsomedial nucleus of the hypothalamus f fornix PT paratenial thalamic nucleus fr fasciculus retroflexus pv periventricular fiber system GP globus pallidus PVA anterior paraventricular thalamic nucleus HDB nucleus of the horizontal limb of the diagonal band PVP posterior paraventricular thalamic nucleus ic internal capsule RCh retrochiasmatic area IGL intergeniculate leaf SC superior colliculus LA lateral nucleus of the amygdala SCh suprachiasmatic nucleus LH lateral hypothalamic area SG suprageniculate nucleus of the thalamus LSd dorsal lateral septum SI substantia innominata LSi intermediate lateral septum sm stria medullaris of thalamus LSv ventral lateral septum SN substantia nigra LP lateral posterior thalamic nucleus SPF subparafascicular nucleus LPO lateral preoptic area SPFPC parvicellular division of the subparafascicular nucleus LV lateral ventricle st stria terminalis MeA medial nucleus of the amygdala StHy striohypothalamic nucleus mfb medial forbrain bundle SuM supramammillary nucleus MGD dorsal division of the medial geniculate nucleus vaf ventral amygdalofugal pathway MGM medial division of the medial geniculate nucleus VMH ventromedial nucleus of the hypothalamus MGV ventral division of the medial geniculate nucleus VP ventral pallidum ml medial lemniscus ZI zona incerta 476 S. CAMPEAU AND S.J. WATSON, JR. Interestingly, rats sustaining disruption (ibotenic acid Committee of the University of Michigan and conformed lesions) of the entire auditory thalamus and of the adja- to NIH guidelines involving vertebrate animals in re- cent multisensory lateral parvicellular division of the sub- search. parafascicular nucleus and posterior intralaminar nu- cleus, display a specific and complete blockade of Noise stress procedure audiogenic stress-induced corticosterone release, as well Prior to perfusion, rats were transferred from the colony as a near complete abolition of c-fos mRNA induction in room to an adjacent room, in their home plastic cages, into stress-responsive
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