Top

Published in:

Open Access 01-01-2019 | Original Article

The orbitofrontal cortex projects to the parvafox nucleus of the ventrolateral hypothalamus and to its targets in the ventromedial periaqueductal grey matter

Authors: Alexandre Babalian, Simone Eichenberger, Alessandro Bilella, Franck Girard, Viktoria Szabolcsi, Diana Roccaro, Gonzalo Alvarez-Bolado, Chun Xu, Marco R. Celio

Published in: Brain Structure and Function | Issue 1/2019

Abstract

Although connections between the orbitofrontal cortex (OFC)—the seat of high cognitive functions—the lateral hypothalamus and the periaqueductal grey (PAG) have been recognized in the past, the precise targets of the descending fibres have not been identified. In the present study, viral tracer-transport experiments revealed neurons of the lateral (LO) and the ventrolateral (VLO) OFC (homologous to part of Area 13 in primates) to project to a circumscribed region in the ventrolateral hypothalamus, namely, the horizontally oriented, cylindrical parvalbumin- and Foxb1-expressing (parvafox) nucleus. The fine collaterals stem from coarse axons in the internal capsule and form excitatory synapses specifically with neurons of the parvafox nucleus, avoiding the rest of the hypothalamus. In its further caudal course, this contingent of LO/VLO-axons projects collaterals to the Su3- and the PV2 nuclei, which lie ventral to the aqueduct in the (PAG), where the terminals fields overlap those deriving from the parvafox nucleus itself. The targeting of the parvafox nucleus by the LO/VLO-projections, and the overlapping of their terminal fields within the PAG, suggest that the two cerebral sites interact closely. An involvement of this LO/VLO-driven circuit in the somatic manifestation of behavioural events is conceivable.

Available only for authorised users

Allen GV, Cechetto DF (1992) Functional and anatomical organization of cardiovascular pressor and depressor sites in the lateral hypothalamic area 1. Descending projections. J Comp Neurol 315(3):313–332CrossRefPubMed

Allen GV, Cechetto DF (1993) Functional and anatomical organization of cardiovascular pressor and depressor sites in the lateral hypothalamic area 2. Ascending projections. J Comp Neurol 330(3):421–438CrossRefPubMed

Alvarez-Bolado G, Zhou X, Cecconi F, Gruss P (2000) Expression of Foxb1 reveals two strategies for the formation of nuclei in the developing ventral diencephalon. Dev Neurosci 22(3):197–206CrossRefPubMed

Bacon SJ, Smith AD (1993) A monosynaptic pathway from an identified vasomotor centre in the medial prefrontal cortex to an autonomic area in the thoracic spinal cord. Neuroscience 54(3):719–728CrossRefPubMed

Bailey P, Sweet WH (1940) Effects on respiration, blood pressure and gastric motility of stimulation of orbital surface of frontal lobe. J Neurophysiol 3(3):276–281CrossRef

Bechara A, Damasio H, Damasio AR (2000) Emotion, decision making and the orbitofrontal cortex. Cereb Cortex 10(3):295–307CrossRefPubMed

Bechara A, Damasio H, Tranel D, Damasio AR (2005) The Iowa Gambling Task and the somatic marker hypothesis: some questions and answers. Trends Cogn Sci 9(4):159–162CrossRefPubMed

Beckstead RM (1979) An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex in the rat. J Comp Neurol 184(1):43–62CrossRefPubMed

Berendse HW, Galis-de Graaf Y, Groenewegen HJ (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316(3):314–347CrossRefPubMed

Bilella A, Alvarez-Bolado G, Celio MR (2014) Coaxiality of Foxb1- and parvalbumin-expressing neurons in the lateral hypothalamic PV1-nucleus. Neurosci Lett 566:111–114CrossRefPubMed

Bilella A, Alvarez-Bolado G, Celio MR (2016) The Foxb1-expressing neurons of the ventrolateral hypothalamic parvafox nucleus project to defensive circuits. J Comp Neurol 524(15):2955–2981CrossRefPubMed

Carmichael ST, Price JL (1994) Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. J Comp Neurol 346(3):366–402CrossRefPubMed

Carmichael ST, Price JL (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 371(2):179–207CrossRefPubMed

Carrive P, Paxinos G (1994) The supraoculomotor cap: a region revealed by NADPH diaphorase histochemistry. Neuroreport 5(17):2257–2260CrossRefPubMed

Celio MR (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231(4741):995–997CrossRefPubMed

Celio MR (1990) Calbindin D-28 k and parvalbumin in the rat nervous system. Neuroscience 35(2):375–475CrossRefPubMed

Celio MR, Babalian A, Ha QH, Eichenberger S, Clement L, Marti C, Saper CB (2013) Efferent connections of the parvalbumin-positive (PV1) nucleus in the lateral hypothalamus of rodents. J Comp Neurol 521(14):3133–3153CrossRefPubMedPubMedCentral

Chamberlin NL, Du B, de Lacalle S, Saper CB (1998) Recombinant adeno-associated virus vector: use for transgene expression and anterograde tract tracing in the CNS. Brain Res 793(1–2):169–175CrossRefPubMedPubMedCentral

Chapman WP, Livingston RB, Livingston KE (1948) The Effect on Respirations and Blood Pressure of Electrical Stimulation of the Orbital Surface of the Frontal Lobe and of Frontal Lobotomy in Man. J Clin Investig 27(4):529–529PubMed

Chen S, Aston-Jones G (1996) Extensive projections from the midbrain periaqueductal gray to the caudal ventrolateral medulla: a retrograde and anterograde tracing study in the rat. Neuroscience 71(2):443–459CrossRefPubMed

Clark Le Gros WE, Meyer M (1950) Anatomical relationships between the cerebral cortex and the hypothalamus. Br Med Bull 6(4):341–345CrossRef

Coffield JA, Bowen KK, Miletic V (1992) Retrograde tracing of projections between the nucleus submedius, the ventrolateral orbital cortex, and the midbrain in the rat. J Comp Neurol 321(3):488–499CrossRefPubMed

Comoli E, Das Neves Favaro P, Vautrelle N, Leriche M, Overton PG, Redgrave P (2012) Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense. Front Neuroanat 6:9CrossRefPubMedPubMedCentral

Craig AD Jr, Wiegand SJ, Price JL (1982) The thalamo-cortical projection of the nucleus submedius in the cat. J Comp Neurol 206(1):28–48CrossRefPubMed

Damasio AR (1996) The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond B Biol Sci 351(1346):1413–1420CrossRefPubMed

Delgado JMR, Mihailovic L, Sevillano M (1960) Cardiovascular Phenomena during Seizure Activity. J Nerv Ment Dis 130(6):477–487CrossRefPubMed

Dong HW (2008) Allen reference atlas: a digital color brain atlas of the C57Bl/6J male mouse. Wiley-Liss

Fernandez De Molina A, Hunsperger RW (1962) Organization of the subcortical system governing defence and flight reactions in the cat. J Physiol 160:200–213CrossRef

Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R (2000) Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol 422(4):556–578CrossRefPubMed

Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R (2001) Orbitomedial prefrontal cortical projections to hypothalamus in the rat. J Comp Neurol 432(3):307–328CrossRefPubMed

Franklin K, Chudasama BJY (2012) Prefrontal cortex. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic Press, Amsterdam

Franklin K, Paxinos BJG (2008) The mouse brain in stereotaxic coordinates. Elsevier, Amsterdam

Fuster JM (2008) The prefrontal cortex. Elsevier Academic Press, AmsterdamCrossRef

Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492(2):145–177CrossRefPubMed

Geerling JC, Kim M, Mahoney CE, Abbott SB, Agostinelli LJ, Garfield AS, Krashes MJ, Lowell BB, Scammell TE (2016) Genetic identity of thermosensory relay neurons in the lateral parabrachial nucleus. Am J Physiol Regul Integr Comp Physiol 310(1):R41–R54CrossRefPubMed

Gelsema AJ, Roe MJ, Calaresu FR (1989) Neurally Mediated Cardiovascular-Responses to Stimulation of Cell-Bodies in the Hypothalamus of the Rat. Brain Res 482(1):67–77CrossRefPubMed

Gerig AT, Celio MR (2007) The human lateral tuberal nucleus: Immunohistochemical characterization and analogy to the rodent PV1-nucleus. Brain Res 1139:110–116CrossRefPubMed

Girard F, Meszar Z, Marti C, Davis FP, Celio M (2011) Gene expression analysis in the parvalbumin-immunoreactive PV1 nucleus of the mouse lateral hypothalamus. Eur J Neurosci 34(12):1934–1943CrossRefPubMed

Gonzalo-Ruiz A, Leichnetz GR (1987) Collateralization of cerebellar efferent projections to the paraoculomotor region, superior colliculus and medial pontine reticular formation in the rat: a fluorescence double-labeling study. Ex Brain Res 68:365–378

Gonzalo-Ruiz A, Leichnetz GR, Hardy SG (1990) Projections of the medial cerebellar nucleus to oculomotor-related midbrain areas in the rat: an anterograde and retrograde HRP study. J Comp Neurol 296(3):427–436CrossRefPubMed

Groenewegen HJ (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24(2):379–431CrossRefPubMed

Groenewegen HJ, Berendse HW, Wolters JG, Lohman AH (1990) The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. Prog Brain Res 85:95–116CrossRefPubMed

Guldin WO, Pritzel M, Markowitsch HJ (1981) Prefrontal cortex of the mouse defined as cortical projection area of the thalamic mediodorsal nucleus. Brain Behav Evol 19(3–4):93–107CrossRefPubMed

Hall RE, Cornish K (1977) Role of orbital cortex in cardiac dysfunction in unanesthetized rhesus-monkey. Exp Neurol 56(2):289–297CrossRefPubMed

Hardy SG (1986) Projections to the midbrain from the medial versus lateral prefrontal cortices of the rat. Neurosci Lett 63(2):159–164CrossRefPubMed

Hardy SG (1994) Anatomical data supporting the concept of prefrontal influences upon hypothalamo-medullary relays in the rat. Neurosci Lett 169(1–2):17–20CrossRefPubMed

Hess WR (1947) Vegetative Funktionen und Zwischenhirn. Helv Physiol et Pharmakol Acta Suppl. IV:1–89

Hess WR (1957) The functional organization of the diencephalon. Hughes JR (ed) New York: Grune & Stratton. 180 p

Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3(5):e159CrossRefPubMedPubMedCentral

Hunsperger RW (1956) Affekreaktionen auf elektrische Reizung im Hirnstamm der Katze. Helv Physiol Acta 14:70–92

Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308(2):249–276CrossRefPubMed

Illig KR (2005) Projections from orbitofrontal cortex to anterior piriform cortex in the rat suggest a role in olfactory information processing. J Comp Neurol 488(2):224–231CrossRefPubMedPubMedCentral

Jasmin L, Burkey AR, Granato A, Ohara PT (2004) Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J Comp Neurol 468(3):425–440CrossRefPubMed

Jones EG, Leavitt RY (1974) Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J Comp Neurol 154(4):349–377CrossRefPubMed

Kaada BR, Jansen J, Andersen P (1953) Stimulation of the hippocampus and medial cortical areas in unanesthetized cats. Neurology 3(11):844–857CrossRefPubMed

Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171(2):157–191CrossRefPubMed

Lee AT, Vogt D, Rubenstein JL, Sohal VS (2014) A class of GABAergic neurons in the prefrontal cortex sends long-range projections to the nucleus accumbens and elicits acute avoidance behavior. J Neurosci 34(35):11519–11525CrossRefPubMedPubMedCentral

Leichnetz GR, Gonzalo-Ruiz A (1987a) Collateralization of frontal eye field (medial precentral/anterior cingulate) neurons projecting to the paraoculomotor region, superior colliculus and medial pontine reticular formation in the rat: a fluorescent double labeling study. Exp Brain Res 68:355–364CrossRefPubMed

Leichnetz GR, Gonzalo-Ruiz A (1987b) Collateralization of frontal eye field (medial precentral/anterior cingulate) neurons projecting to the paraoculomotor region, superior colliculus, and medial pontine reticular formation in the rat: a fluorescent double-labeling study. Exp Brain Res 68(2):355–364CrossRefPubMed

Leichnetz GR, Hardy SG, Carruth MK (1987a) Frontal projections to the region of the oculomotor complex in the rat: a retrograde and anterograde HRP study. J Comp Neurol 263(3):387–399CrossRefPubMed

Leichnetz GR, Hardy SGP, Carruth MK (1987b) Frontal Projections to the region of the oculomotor complex in the rat—a retrograde and anterograde Hrp study. J Comp Neurol 263(3):387–399CrossRefPubMed

Leonard CM (1969) Prefrontal cortex of rat. I. Cortical Projection of Mediodorsal Nucleus .2. Efferent Connections. Brain Res 12(2):321CrossRefPubMed

Loewy AD (1991) Forebrain nuclei involved in autonomic control. Prog Brain Res 87:253–268CrossRefPubMed

McDonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71(1):55–75CrossRefPubMed

Meszar Z, Girard F, Saper CB, Celio MR (2012) The lateral hypothalamic parvalbumin-immunoreactive (PV1) nucleus in rodents. J Comp Neurol 520(4):798–815CrossRefPubMedPubMedCentral

Ogawa SK, Cohen JY, Hwang D, Uchida N, Watabe-Uchida M (2014) Organization of monosynaptic inputs to the serotonin and dopamine neuromodulatory systems. Cell Rep 8(4):1105–1118CrossRefPubMedPubMedCentral

Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508(7495):207–214CrossRefPubMedPubMedCentral

Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10(3):206–219CrossRefPubMed

Ongur D, An X, Price JL (1998) Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 401(4):480–505CrossRefPubMed

Ongur D, Ferry AT, Price JL (2003) Architectonic subdivision of the human orbital and medial prefrontal cortex. J Comp Neurol 460(3):425–449CrossRefPubMed

Paxinos G, Franklin K, B.,J (2013) The mouse brain in stereotaxic coordinates. Elsevier, Amsterdam

Pickering TG, Devereux RB, James GD, Gerin W, Landsbergis P, Schnall PL, Schwartz JE (1996) Environmental influences on blood pressure and the role of job strain. J Hypertens Suppl 14(5):S179–S185PubMed

Price JL (1985) Beyond the primary olfactory cortex—olfactory-related areas in the neocortex, thalamus and hypothalamus. Chem Senses 10(2):239–258CrossRef

Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann NY Acad Sci 1121:54–71CrossRefPubMed

Price JL, Slotnick BM (1983) Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study. J Comp Neurol 215(1):63–77CrossRefPubMed

Price JL, Slotnick BM, Revial MF (1991) Olfactory projections to the hypothalamus. J Comp Neurol 306(3):447–461CrossRefPubMed

Rainville P, Bechara A, Naqvi N, Damasio AR (2006) Basic emotions are associated with distinct patterns of cardiorespiratory activity. Int J Psychophysiol 61(1):5–18CrossRefPubMed

Ray JP, Price JL (1993) The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 337(1):1–31CrossRefPubMed

Reep RL, Corwin JV, King V (1996) Neuronal connections of orbital cortex in rats: topography of cortical and thalamic afferents. Exp Brain Res 111(2):215–232CrossRefPubMed

Reynolds SM, Zahm DS (2005) Specificity in the projections of prefrontal and insular cortex to ventral striatopallidum and the extended amygdala. J Neurosci 25(50):11757–11767CrossRefPubMedPubMedCentral

Rolls ET (2000) The orbitofrontal cortex and reward. Cereb Cortex 10(3):284–294CrossRefPubMed

Ruggiero DA, Mraovitch S, Granata AR, Anwar M, Reis DJ (1987) A role of insular cortex in cardiovascular function. J Comp Neurol 257(2):189–207CrossRefPubMed

Sachs E, Brendler SJ, Fulton JF (1949) The Orbital Gyri Brain 72(2):227–240

Schilman EA, Uylings HB, Galis-de Graaf Y, Joel D, Groenewegen HJ (2008) The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci Lett 432(1):40–45CrossRefPubMed

Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10(3):272–284CrossRefPubMed

Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290(2):213–242CrossRefPubMed

Spencer WG (1894) The effect produced upon respiration by faradic excitation of the cerebrum in the monkey, dog, cat and rabbit. Philos Trans B 185:609–657CrossRef

Swanson LW (2004) Brain maps: the structure of the rat brain. Elsevier Academic Press, San Diego

Takagishi M, Chiba T (1991) Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res 566(1–2):26–39CrossRefPubMed

Tamamaki N, Tomioka R (2010) Long-Range GABAergic Connections Distributed throughout the Neocortex and their Possible Function. Front Neurosci 4:202CrossRefPubMedPubMedCentral

Van Bockstaele EJ, Pieribone VA, Aston-Jones G (1989) Diverse afferents converge on the nucleus paragigantocellularis in the rat ventrolateral medulla: retrograde and anterograde tracing studies. J Comp Neurol 290(4):561–584CrossRefPubMed

Verberne AJM (1996) Medullary sympathoexcitatory neurons are inhibited by activation of the medial prefrontal cortex in the rat. Am J Physiol-Reg I 270(4):R713–R719

Verberne AJM, Owens NC (1998) Cortical modulation of the cardiovascular system. Prog Neurobiol 54(2):149–168CrossRefPubMed

Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51(1):32–58CrossRefPubMed

Wall NR, Wickersham IR, Cetin A, De La Parra M, Callaway EM (2010) Monosynaptic circuit tracing in vivo through Cre-dependent targeting and complementation of modified rabies virus. Proc Natl Acad Sci U S A 107(50):21848–21853CrossRefPubMedPubMedCentral

Ward AA, McCulloch WS (1947) The projection of the frontal lobe on the hypothalamus. J Neurophysiol 10(4):309–314CrossRefPubMed

Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N (2012) Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74(5):858–873CrossRefPubMed

Wickersham IR, Finke S, Conzelmann KK, Callaway EM (2007a) Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4(1):47–49CrossRefPubMed

Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, Young JA, Callaway EM (2007b) Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53(5):639–647CrossRefPubMedPubMedCentral

Wyss JM, Sripanidkulchai K (1984) The topography of the mesencephalic and pontine projections from the cingulate cortex of the rat. Brain Res 293(1):1–15CrossRefPubMed

Yasui Y, Breder CD, Saper CB, Cechetto DF (1991) Autonomic responses and efferent pathways from the insular cortex in the rat. Journal of Comparative Neurology 303(3):355–374CrossRefPubMed

Yoshida A, Dostrovsky JO, Chiang CY (1992) The afferent and efferent connections of the nucleus submedius in the rat. J Comp Neurol 324(1):115–133CrossRefPubMed

Zhang X, Hannesson DK, Saucier DM, Wallace AE, Howland J, Corcoran ME (2001) Susceptibility to kindling and neuronal connections of the anterior claustrum. J Neurosci 21(10):3674–3687CrossRefPubMedPubMedCentral

Zhao T, Zhou X, Szabo N, Leitges M, Alvarez-Bolado G (2007) Foxb1-driven Cre expression in somites and the neuroepithelium of diencephalon, brainstem, and spinal cord. Genesis 45(12):781–787CrossRefPubMed

Title: The orbitofrontal cortex projects to the parvafox nucleus of the ventrolateral hypothalamus and to its targets in the ventromedial periaqueductal grey matter
Authors: Alexandre Babalian
Simone Eichenberger
Alessandro Bilella
Franck Girard
Viktoria Szabolcsi
Diana Roccaro
Gonzalo Alvarez-Bolado
Chun Xu
Marco R. Celio
Publication date: 01-01-2019
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2019
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1771-5

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

The orbitofrontal cortex projects to the parvafox nucleus of the ventrolateral hypothalamus and to its targets in the ventromedial periaqueductal grey matter

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

Topological principles and developmental algorithms might refine diffusion tractography

Meta-analysis of functional subdivisions within human posteromedial cortex

Medium spiny neurons of the anterior dorsomedial striatum mediate reversal learning in a cell-type-dependent manner

Aldosterone-sensitive HSD2 neurons in mice

Unidirectional monosynaptic connections from auditory areas to the primary visual cortex in the marmoset monkey

The SLC6A3 3′-UTR VNTR and intron 8 VNTR polymorphisms association in the time estimation