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The rostromedial zona incerta is involved in attentional processes while adjacent LHA responds to arousal: c-Fos and anatomical evidence

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Abstract

Neurons producing melanin-concentrating hormone (MCH) are located in the tuberal lateral hypothalamus (LHA) and in the rostromedial part of the zona incerta (ZI). This distribution suggests that rostromedial ZI shares some common features with the LHA. However, its functions with regard to arousal or feeding, which are often associated with the LHA, have not been thoroughly investigated. This study analyses the responses in the tuberal LHA and adjacent rostromedial ZI after experiments related to arousal, exploration, food teasing and ingestive behavior. Specific aspects of the connections of the rostromedial ZI were also studied using retrograde and anterograde tract-tracing approaches. The rostromedial ZI is activated during exploratory and teasing experiments. It receives specific projections from the frontal eye field and the anterior pole of the superior colliculus that are involved in gaze fixation and saccadic eye movements. It also receives projections from the laterodorsal tegmental nucleus involved in attention/arousal. By contrast, the tuberal LHA is activated during wakefulness and exploratory behavior and reportedly receives projections from the medial prefrontal and insular cortex, and from several brainstem structures such as the periaqueductal gray. We conclude that the rostromedial ZI is involved in attentional processes while the adjacent tuberal LHA is involved in arousal.

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Abbreviations

ACAd:

Anterior cingulate area, dorsal part

ACB:

Nucleus accumbens

ac:

Anterior commissure

aco:

Anterior commissure, olfactory limb

AD:

Anterodorsal nucleus thalamus

AHN:

Anterior hypothalamic nucleus

AId:

Agranular insular area, dorsal part

AM:

Anteromedial nucleus thalamus

AMd:

Anteromedial nucleus thalamus, dorsal part

AP:

Anteroposterior

APN:

Anterior pretectal nucleus

AQ:

Cerebral aqueduct proper

ARH:

Arcuate hypothalamic nucleus

AV:

Anteroventral nucleus thalamus

BLA:

Basolateral amygdalar nucleus

BST:

Bed nuclei stria terminalis

C:

Control rat

CEA:

Central amygdalar nucleus

CL:

Central lateral nucleus thalamus

CLA:

Claustrum

CM:

Central medial nucleus thalamus

CP:

Caudoputamen

cpd:

Cerebral peduncle

CRH:

Corticotropin-releasing hormone

CS:

Superior central nucleus raphé

cst:

Corticospinal tract

CUN:

Cuneiform nucleus

DAB:

Diaminobenzidine

DMH:

Dorsomedial hypothalamic nucleus

DMHa:

Dorsomedial hypothalamic nucleus, anterior part

DMHp:

Dorsomedial hypothalamic nucleus, posterior part

DMHv:

Dorsomedial hypothalamic nucleus, ventral part

DR:

Dorsal nucleus raphé

DV:

Dorsoventral

fa:

Corpus callosum, anterior forceps

FEF:

Frontal eye field

FF:

Fields of Forel

FG:

Fluorogold

FL:

Flocculus

fr:

Fasciculus retroflexus

fx:

Columns of the fornix

GABA:

Gamma-aminobutyric acid

GP:

Globus pallidus

GU:

Gustatory area

Hcrt:

Hypocretin

HRP:

Horseradish peroxidase

ICe:

Inferior colliculus, external nucleus

ILA:

Infralimbic area

IMD:

Intermediodorsal nucleus thalamus

int:

Internal capsule

IP:

Intraperitoneal

IPN:

Interpeduncular nucleus

LD:

Lateral dorsal nucleus thalamus

LDT:

Laterodorsal tegmental nucleus

LG:

Lateral geniculate complex

LH:

Lateral habenula

LHA:

Lateral hypothalamic area

LM:

Lateral mammillary nucleus

LP:

Lateral posterior nucleus thalamus

MA:

Magnocellular nucleus

MCH:

Melanin-concentrating hormone

MD:

Mediodorsal nucleus thalamus

ME:

Median eminence

MG:

Medial geniculate complex

ML:

Mediolateral

MM:

Medial mammillary nucleus, body

MOp:

Primary somatomotor area

MOs:

Secondary somatomotor areas

MPN:

Medial preoptic nucleus

MPT:

Medial pretectal area

MRN:

Midbrain reticular nucleus

mtt:

Mammillothalamic tract

N:

Naïve rat

Nc:

Cage naïve rat

NLL:

Nucleus of the lateral lemniscus

Nn:

Night naïve rat

NOT:

Nucleus of the optic tract

NPC:

Nucleus of the posterior commissure

opt:

Optic tract

OT:

Olfactory tubercle

PAG:

Periaqueductal gray

PB:

Parabrachial nucleus

PBS:

Phosphate buffered saline

PBS-T:

Phosphate buffered saline with triton

PF:

Parafascicular nucleus

PFA:

Paraformaldehyde

PG:

Pontine gray

PH:

Posterior hypothalamic nucleus

PHA-L:

Phaseolus vulgaris leucoagglutinin

PIR:

Piriform area

PL:

Prelimbic area

pm:

Principal mammillary tract

PMd:

Dorsal premammillary nucleus

PMv:

Ventral premammillary nucleus

PO:

Posterior complex thalamus

POA:

Preoptic area

PP:

Peripeduncular nucleus

PPN:

Pedunculopontine nucleus

PPT:

Posterior pretectal nucleus

PR:

Perireuniens nucleus

PRC:

Precommissural nucleus, periaqueductal gray

PRN:

Pontine reticular nucleus

PSV:

Principal sensory nucleus of the trigeminal

PVH:

Paraventricular hypothalamic nucleus

PVT:

Paraventricular thalamic nucleus

py:

Pyramid

RE:

Nucleus reuniens

REa:

Nucleus reuniens, rostral division, anterior part

RH:

Rhomboid nucleus

RL:

Rostral linear nucleus raphé

RM:

Nucleus raphé magnus

RN:

Red nucleus

ROI:

Region of interest

RR:

Midbrain reticular nucleus, retrorubral area

RS:

Re-fed rat

RT:

Reticular nucleus thalamus

SC:

Superior colliculus

SCH:

Suprachiasmatic nucleus

SCig:

Superior colliculus, intermediate gray layer

SF:

Septofimbrial nucleus

SI:

Substantia innominata

sm:

Stria medullaris

SMT:

Submedial nucleus thalamus

SN:

Substantia nigra

SNr:

Substantia nigra, reticular part

SSp:

Primary somatosensory area

STN:

Subthalamic nucleus

SUM:

Supramammillary nucleus

SUMl:

Supramammillary nucleus, lateral part

T:

Teased rat

TT:

Tenia tecta

V3:

Third ventricle

V4:

Fourth ventricle

VAL:

Ventral anterior-lateral complex thalamus

VL:

Lateral ventricle

vlt:

Ventrolateral tract

VM:

Ventral medial nucleus thalamus

VMH:

Ventromedial hypothalamic nucleus

VPL:

Ventral posterolateral nucleus thalamus

VPM:

Ventral posteromedial nucleus thalamus

VTA:

Ventral tegmental area

ZI:

Zona incerta

ZIda:

Zona incerta, dopaminergic group

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Acknowledgements

This research was supported by funding from the French Ministère de la Recherche et de la Technologie (EA 3922) and from the Région de Franche-Comté. The authors want to thank Frances Thivet for the help in the preparation of the manuscript.

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Correspondence to P. Y. Risold.

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Movie S1 During the feeding procedure, the teased rat previously deprived of food during 24h spent most of the one hour experiment trying to reach the food inside the meshed box while the control rat rested in the cage. (MOV 2258 KB)

Movie S1 During the feeding procedure, the teased rat previously deprived of food during 24h spent most of the one hour experiment trying to reach the food inside the meshed box while the control rat rested in the cage. (MOV 2258 KB)

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Chometton, S., Charrière, K., Bayer, L. et al. The rostromedial zona incerta is involved in attentional processes while adjacent LHA responds to arousal: c-Fos and anatomical evidence. Brain Struct Funct 222, 2507–2525 (2017) doi:10.1007/s00429-016-1353-3

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Keywords

  • Frontal eye field
  • Superior colliculus
  • Laterodorsal tegmental nucleus
  • Dorsomedial nucleus