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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
Institution: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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