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Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat
Authors:Joel D. Hahn  Larry W. Swanson
Affiliation:Department of Biological Sciences, University of Southern California, Los Angeles, CA 90089-2520, USA
Abstract:We have analyzed at high resolution the neuroanatomical connections of the juxtaparaventricular region of the lateral hypothalamic area (LHAjp); as a control and in comparison to this, we also performed a preliminary analysis of a nearby LHA region that is dorsal to the fornix, namely the LHA suprafornical region (LHAs). The connections of these LHA regions were revealed with a coinjection tract-tracing technique involving a retrograde (cholera toxin B subunit) and anterograde (Phaseolus vulgaris leucoagglutinin) tracer. The LHAjp and LHAs together connect with almost every major division of the cerebrum and cerebrospinal trunk, but their connection profiles are markedly different and distinct. In simple terms, the connections of the LHAjp indicate a possible primary role in the modulation of defensive behavior; for the LHAs, a role in the modulation of ingestive behavior is suggested. However, the relation of the LHAjp and LHAs to potential modulation of these behaviors, as indicated by their neuroanatomical connections, appears to be highly integrative as it includes each of the major functional divisions of the nervous system that together determine behavior, i.e., cognitive, state, sensory, and motor. Furthermore, although a primary role is indicated for each region with respect to a particular mode of behavior, intermode modulation of behavior is also indicated. In summary, the extrinsic connections of the LHAjp and LHAs (so far as we have described them) suggest that these regions have a profoundly integrative role in which they may participate in the orchestrated modulation of elaborate behavioral repertoires.
Keywords:AAA, anterior amygdalar area   ACAd, anterior cingulate area, dorsal part   ACAv, anterior cingulate area, ventral part   ACB, nucleus accumbens (&ldquo  shell&rdquo   region)   aco, anterior commissure, olfactory limb   act, anterior commissure, temporal limb   AD, anterodorsal nucleus thalamus   ADP, anterodorsal preoptic nucleus   AHA, anterior hypothalamic area   AHNa, anterior hypothalamic nucleus, anterior part   AHNc, anterior hypothalamic nucleus, central part   AHNd, anterior hypothalamic nucleus, dorsal part   AHNp, anterior hypothalamic nucleus, posterior part   Ald, agranular insular area, dorsal part   Alp, agranular insular area, posterior part   Alv, agranular insular area, ventral part   alv, alveus of fornix   AMd, anteromedial nucleus thalamus, dorsal part   AMv, anteromedial nucleus thalamus, ventral part   AONpv, anterior olfactory nucleus, posteroventral part   AP, area postrema   AQ, cerebral aqueduct   AQc, cerebral aqueduct collicular recess   ARH, arcuate hypothalamic nucleus   AT, anterior tegmental nucleus   AV, anteroventral nucleus thalamus   AVP, anteroventral preoptic nucleus   AVPV, anteroventral periventricular nucleus   B, Barrington's nucleus   BA, bed nucleus of the accessory olfactory part   BAC, bed nucleus anterior commissure   BLAp, basolateral amygdalar nucleus, posterior part   BMAa, basomedial amygdalar nucleus, anterior part   BSM, bed nucleus of the stria medullaris   BSTal, bed nuclei stria terminalis, anterior division, anterolateral area   BSTam, bed nuclei stria terminalis, anterior division, anteromedial area   BSTd, bed nuclei stria terminalis, posterior division, dorsal nucleus   BSTdm, bed nuclei stria terminalis, anterior division, dorsomedial nucleus   BSTfu, bed nuclei stria terminalis, anterior division, fusiform nucleus   BSTif, bed nuclei stria terminalis, posterior division, interfascicular nucleus   BSTmg, bed nuclei stria terminalis, anterior division, magnocellular nucleus   BSTpr, bed nuclei stria terminalis, posterior division, principal nucleus   BSTse, bed nuclei stria terminalis, anterior division, rhomboid nucleus   BSTtr, bed nuclei stria terminalis, posterior division, transverse nucleus   BSTv, bed nuclei stria terminalis, anterior division, ventral nucleus   C, central canal   CA1, field CA1, Ammon's horn   CA1so, field CA1, stratum oriens   CA1spd, field CA1, pyramidal layer, deep   CA1sps, field CA1, pyramidal layer, superficial   CA2sp, field CA2, pyramidal layer   CA3so, field CA3, stratum oriens   CA3sp, field CA3, pyramidal layer   cc, corpus callosum   ccg, genu of corpus callosum   CEAc, central amygdalar nucleus, capsular part   CEAl, central amygdalar nucleus, lateral part   CEAm, central amygdalar nucleus, medial part   cic, commissure of the inferior colliculus   cing, cingulum bundle   CL, central lateral nucleus thalamus   CLA, claustrum   CLI, central linear nucleus raphé     CM, central medial nucleus thalamus   COAa, cortical amygdalar area, anterior part   COApl, cortical amygdalar area, posterior part, lateral zone   COApm, cortical amygdalar area, posterior part, medial zone   COM, periaqueductal gray, commissural nucleus   CP, caudoputamen   cpd, cerebral peduncle   csc, commissure of the superior colliculus   CSl, superior central nucleus raphé  , lateral part   CSm, superior central nucleus raphé  , medial part   CUN, cuneiform nucleus   da, dopamine (cell group within zona incerta)   DCO, dorsal cochlear nucleus   df, dorsal fornix   DGlb, dentate gyrus lateral blade   DMHa, dorsomedial hypothalamic nucleus, anterior part   DMHp, dorsomedial hypothalamic nucleus, posterior part   DMHv, dorsomedial hypothalamic nucleus, ventral part   DMX, dorsal motor nucleus vagus nerve   DR, dorsal nucleus raphé     dscp, decussation of the superior cerebellar peduncle   DTN, dorsal tegmental nucleus   ec, corpus callosum external capsule   ee, corpus callosum extreme capsule   em, external medullary lamina thalamus   ENTl, entorhinal area, lateral part   ENTm, entorhinal area, medial part, dorsal zone   EPd, endopiriform nucleus, dorsal part   EW, Edinger-Westphal nucleus   fa, corpus callosum anterior forceps   FF, fields of Forel   fi, fimbria   fr, fasciculus retroflexus   FS, fundus of the striatum   fx, columns of the fornix   fxpr, precommissural fornix   GPe, globus pallidus, external segment   GPi, globus pallidus, internal segment   GR, gracile nucleus   GRN, gigantocellular reticular nucleus   gVIIn, genu of the facial nerve   hbc, habenular commissure   HPF, hippocampal formation   I, internuclear area, hypothalamic periventricular region   IA, intercolated nuclei amygdala   IAD, interanterodorsal nucleus thalamus   IAM, interanteromedial nucleus thalamus   ICc, inferior colliculus central nucleus   ICd, inferior colliculus dorsal nucleus   ICe, inferior colliculus external nucleus   IF, interfascicular nucleus raphé     IG, induseum griseum   ILA, infralimbic area   im, internal medullary lamina thalamus   IMD, intermediodorsal nucleus thalamus   INC, interstitial nucleus of Cajal   int, internal capsule   IPNc, interpeduncular nucleus central subnucleus   IPNd, interpeduncular nucleus dorsomedial subnucleus   IPNi, interpeduncular nucleus intermediate subnucleus   IPNld, interpeduncular nucleus lateral subnucleus dorsal part   IPNli, interpeduncular nucleus, lateral subnucleus, intermediate part   IPNlr, interpeduncular nucleus lateral subnucleus rostral part   IPNr, interpeduncular nucleus rostral subnucleus   ISN, inferior salivatory nucleus   ivf, interventricular foramen   KF, Kolliker-Fuse subnucleus   LC, locus ceruleus   LD, lateral dorsal nucleus thalamus   LDT, laterodorsal tegmental nucleus   LGd, dorsal part of the lateral geniculate complex   LH, lateral habenula   LHAad, lateral hypothalamic area, anterior region, dorsal zone   LHAai, lateral hypothalamic area, anterior region, intermediate zone   LHAav, lateral hypothalamic area, anterior region, ventral zone   LHAd, lateral hypothalamic area, dorsal region   LHAjd, lateral hypothalamic area, juxtadorsomedial region   LHAjp, lateral hypothalamic area, juxtaparaventricular region   LHAjvd, lateral hypothalamic area, juxtaventromedial region, dorsal zone   LHAjvv, lateral hypothalamic area, juxtaventromedial region, ventral zone   LHAm, lateral hypothalamic area, magnocellular nucleus   LHAmo, lateral hypothalamic area, motor related   LHAp, lateral hypothalamic area, posterior region   LHApc, lateral hypothalamic area, parvicellular region   LHAs, lateral hypothalamic area, suprafornical region   LHAsfa, lateral hypothalamic area, subfornical region, anterior zone   LHAsfp, lateral hypothalamic area, subfornical region, posterior zone   LHAsfpm, lateral hypothalamic area, subfornical region, premammillary zone   LHAvl, lateral hypothalamic area, ventral region, lateral zone   LHAvm, lateral hypothalamic area, ventral region, medial zone   LP, lateral posterior nucleus thalamus   LPO, lateral preoptic area   LRNm, lateral reticular nucleus magnocellular part   LSc.d.d, lateral septal nucleus, caudal (caudodorsal) part, dorsal zone, dorsal region   LSc.d.l, lateral septal nucleus, caudal (caudodorsal) part, dorsal zone, lateral region   LSc.d.r, lateral septal nucleus, caudal (caudodorsal) part, dorsal zone, rostral region   LSc.d.v, lateral septal nucleus, caudal (caudodorsal) part, dorsal zone, ventral region   LSc.v.i, lateral septal nucleus, caudal (caudodorsal) part, ventral zone, intermediate region   LSc.v.l.d, lateral septal nucleus, caudal (caudodorsal) part, ventral zone, lateral region, dorsal domain   LSc.v.l.v, lateral septal nucleus, caudal (caudodorsal) part, ventral zone, lateral region, ventral domain   LSc.v.m.d, lateral septal nucleus, caudal (caudodorsal) part, ventral zone, medial region, dorsal domain   LSc.v.m.v, lateral septal nucleus, caudal (caudodorsal) part, ventral zone, medial region, ventral domain   LSr.dl.l.d, lateral septal nucleus, rostral (rostroventral) part, dorsolateral zone, lateral region, dorsal domain   LSr.dl.l.v, lateral septal nucleus, rostral (rostroventral) part, dorsolateral zone, lateral region, ventral domain   LSr.dl.m.d, lateral septal nucleus, rostral (rostroventral) part, dorsolateral zone, medial region, dorsal domain   LSr.dl.m.v, lateral septal nucleus, rostral (rostroventral) part, dorsolateral zone, medial region, ventral domain   LSr.m.d, lateral septal nucleus, rostral (rostroventral) part, medial zone, dorsal region   LSr.m.v.c, lateral septal nucleus, rostral (rostroventral) part, medial zone, ventral region, caudal domain   LSr.m.v.r, lateral septal nucleus, rostral (rostroventral) part, medial zone, ventral region, rostral domain   LSr.vl.d, lateral septal nucleus, rostral (rostroventral) part, ventrolateral zone, dorsal region   LSr.vl.d.l, lateral septal nucleus, rostral (rostroventral) part, ventrolateral zone, dorsal region, lateral domain   LSr.vl.d.m, lateral septal nucleus, rostral (rostroventral) part, ventrolateral zone, dorsal region, medial domain   LSr.vl.v, lateral septal nucleus, rostral (rostroventral) part, ventrolateral zone, ventral region   LSv, lateral septal nucleus, ventral part   LTN, lateral tegmental nucleus   MA, magnocellular preoptic nucleus   MARN, magnocellular reticular nucleus   mct, medial corticohypothalamic tract   MDc, mediodorsal nucleus thalamus, central part   MDl, mediodorsal nucleus thalamus, lateral part   MDm, mediodorsal nucleus thalamus, medial part   MDRNd, medullary reticular nucleus, dorsal part   MDRNv, medullary reticular nucleus, ventral part   MEAad, medial amygdalar nucleus, anterodorsal part   MEAav, medial amygdalar nucleus, anteroventral part   MEApd-a, medial amygdalar nucleus, posterodorsal part, sublayer a   MEApd-b, medial amygdalar nucleus, posterodorsal part, sublayer b   MEApd-c, medial amygdalar nucleus, posterodorsal part, sublayer c   MEApv, medial amygdalar nucleus, posteroventral part   MEex, median eminence external   MEin, median eminence internal   MEPO, median preoptic nucleus   MEV, mesencephalic nucleus of the trigeminal   MH, medial habenula   ml, medial lemniscus   mlf, medial longitudinal fascicle   MM, medial mammillary nucleus (body)   MMme, medial mammillary nucleus, median part   MO, secondary somatomotor area   moV, motor root of the trigeminal nerve   mp, mammillary peduncle   MPNc, central part   MPNl, medial preoptic nucleus, lateral part   MPNm, medial part   MPO, medial preoptic area   MPT, medial pretectal area   MRNm, midbrain reticular nucleus, magnocellular part   MRNp, midbrain reticular nucleus, parvicellular part   MS, medial septal nucleus   mtg, mammillotegmental tract   mtt, mammillothalamic tract   mtV, mesencephalic tract of the trigeminal nerve   MV, medial vestibular nucleus   NC, supraoptic nucleus, accessory supraoptic group, nucleus circularis   ND, nucleus of Darkschewitsch   NDB, diagonal band nucleus   NIc, nucleus incertus, compact part   NId, nucleus incertus, diffuse part   NIS, nucleus intercalatus   NLOT, nucleus of the lateral olfactory tract   NPC, nucleus of the posterior commissure   NTB, nucleus of the trapezoid body   NTSco, nucleus of the solitary tract, commissural part   NTSl, nucleus of the solitary tract, lateral part   NTSmc, nucleus of the solitary tract, medial part, caudal zone   NTSmr, nucleus of the solitary tract, medial part, rostral zone   och, optic chiasm   opt, optic tract   ORBl, orbital area, lateral part   ORBm, orbital area, medial part   ORBv, ventral part   ORBvl, ventrolateral part   OT, olfactory tubercle   PA, posterior amygdalar nucleus   PAGd, periaqueductal gray, dorsal division   PAGdl, periaqueductal gray, dorsolateral division   PAGm, periaqueductal gray, medial division   PAGrl, periaqueductal gray, rostrolateral division   PAGrm, periaqueductal gray, rostromedial division   PAGvl, periaqueductal gray, ventrolateral division   PAR, parasubiculum   PARN, parvicellular reticular nucleus   PAT, paratrigeminal nucleus   PBlc, parabrachial nucleus, lateral division, central lateral part   PBld, parabrachial nucleus, lateral division, dorsal lateral part   PBle, parabrachial nucleus, lateral division, external lateral part   PBlv, parabrachial nucleus, lateral division, ventral part   PBmm, parabrachial nucleus, medial division, medial part   pc, posterior commissure   PCG, pontine central gray   PF, parafascicular nucleus   PG, pontine gray   PGRNd, paragigantocellular reticular nucleus, dorsal part   PGRNl, paragigantocellular reticular nucleus, lateral part   PH, posterior hypothalamic nucleus   PIR, piriform area   PL, prelimbic area   pm, principal mammillary tract   PMd, dorsal premammillary nucleus   PMv, ventral premammillary nucleus   POR, superior olivary complex periolivary region   POST, postsubiculum   PPN, pedunculopontine nucleus   PPT, posterior pretectal nucleus   PPYd, parapyramidal nucleus, deep part   PR, perireuniens nucleus   PRC, periaqueductal gray, precommissural nucleus   PRE, presubiculum   PRNc, pontine reticular nucleus, caudal part   PRNr, pontine reticular nucleus, rostral part   PRP, nucleus prepositus   PS, parastrial nucleus   PSCH, suprachiasmatic preoptic nucleus   PST, preparasubthalamic nucleus   PSTN, parasubthalamic nucleus   PT, paratenial nucleus   PVa, periventricular hypothalamic nucleus, anterior part   PVHam, paraventricular nucleus hypothalamus, magnocellular division, anterior magnocellular part   PVHap, paraventricular nucleus hypothalamus, anterior parvicellular part   PVHdp, paraventricular nucleus hypothalamus, dorsal parvicellular part   PVHf, paraventricular nucleus hypothalamus, forniceal part   PVHlp, paraventricular nucleus hypothalamus, lateral parvicellular part   PVHmpd, paraventricular nucleus hypothalamus, medial parvicellular part, dorsal zone   PVHmpdl, paraventricular nucleus hypothalamus, medial parvicellular part, dorsal zone, lateral wing   PVHpml, paraventricular nucleus hypothalamus, posterior magnocellular part, lateral zone   PVHpmm, paraventricular nucleus hypothalamus, posterior magnocellular part, medial zone   PVHpv, paraventricular nucleus hypothalamus, periventricular part   PVi, periventricular nucleus hypothalamus, intermediate part   PVp, periventricular nucleus hypothalamus, posterior part   PVpo, preoptic periventricular nucleus   PVT, paraventricular nucleus thalamus   py, pyramidal tract, crossed   RCH, retrochiasmatic area   REa, nucleus reuniens, rostral division, anterior part   REc, nucleus reuniens, caudal division, caudal part   REcd, nucleus reuniens, caudal division, dorsal part   REcm, nucleus reuniens, caudal division, median part   REcp, nucleus reuniens, caudal division, posterior part   REd, nucleus reuniens, rostral division, dorsal part   REl, nucleus reuniens, rostral division, lateral part   REm, nucleus reuniens, rostral division, median part   REv, nucleus reuniens, rostral division, ventral part   RH, rhomboid nucleus   RL, rostral linear nucleus raphé     RM, nucleus raphé   magnus   RN, red nucleus   RO, nucleus raphé   obscurus   RPA, nucleus raphé   pallidus   RR, midbrain reticular nucleus, retrorubral area   RSPv, retrosplenial area, ventral part   RT, reticular nucleus thalamus   rust, rubrospinal tract   SBPV, subparaventricular zone   SCdg, superior colliculus, deep gray layer   SCdg, superior colliculus, deep gray layer   SCH, suprachiasmatic nucleus   SCig-a, superior colliculus, intermediate gray layer, sublayer a   SCig-b, superior colliculus, intermediate gray layer, sublayer b   SCig-c, superior colliculus, intermediate gray layer, sublayer c   scp, superior cerebellar peduncle   SCsg, superior colliculus, superficial gray layer   sctv, ventral spinocerebellar tract   SEZ/RC, subependymal zone/rhinocele   SF, septofimbral nucleus   SFO, subfornical organ   SH, septohippocampal nucleus   SI, substantia innominata   SLD, sublaterodorsal nucleus   sm, stria medullaris   smd, supramammillary decussation   SMT, submedial nucleus of the thalamus   SO, supraoptic nucleus   SPFm, subparafascicular nucleus thalamus, magnocellular part   SPFpl, subparafascicular nucleus thalamus, parvicellular part, lateral division   SPVI, spinal nucleus of the trigeminal interpolar part   SPVOmdmd, spinal nucleus of the trigeminal oral part middle dorsomedial part, dorsal zone   SPVOvl, spinal nucleus of the trigeminal oral part ventrolateral part   st, stria terminalis   SUB-sp1, subiculum, pyramidal layer   SUMl, supramammillary nucleus, lateral part   SUMm, supramammillary nucleus, medial part   sup, supraoptic commissures   SUT, supratrigeminal nucleus   SUV, superior vestibular nucleus   tb, trapezoid body   TMd, tuberomammillary nucleus dorsal part   TMv, tuberomammillary nucleus ventral part   tp, thalamic peduncles   TR, postpiriform transition area   TRN, tegmental reticular nucleus   TRS, triangular nucleus septum   ts, solitary tract   tsp, tectospinal pathway   TTd, tenia tecta, dorsal part   TTv, tenia tecta, ventral part   TUi, tuberal nucleus, intermediate part   TUl, tuberal nucleus, lateral part   TUsv, tuberal nucleus, subventromedial part   TUte, tuberal nucleus, terete subnucleus   V3h, third ventricle, hypothalamic part   V3m, third ventricle mammillary recess   V3p, third ventricle preoptic recess   V3r, third ventricle periventricular recess   V3t, third ventricle, thalamic part   V4, fourth ventricle   VAL, ventral anterior-lateral complex of the thalamus   vhc, ventral hippocampal commissure   VL, lateral ventricle   VLP, ventrolateral preoptic nucleus   vlt, ventrolateral hypothalamic tract   VM, ventral medial nucleus of the thalamus   Vma, motor nucleus of the trigeminal, magnocellular part   VMHa, ventromedial nucleus hypothalamus, anterior part   VMHc, ventromedial nucleus hypothalamus, central part   VMHdm, ventromedial nucleus hypothalamus, dorsomedial part   VMHvl, ventromedial nucleus hypothalamus, ventrolateral part   VPMpc, ventral posteromedial nucleus of the thalamus parvicellular part   VTA, ventral tegmental area   VTN, ventral tegmental nucleus   XII, hypoglossal nucleus   ZI, zona incerta
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