A GABAergic nigrotectal pathway for coordination of drinking behavior
Mark A Rossi, Haofang E Li, Dongye Lu, Il Hwan Kim, Ryan A Bartholomew, Erin Gaidis, Joseph W Barter, Namsoo Kim, Min Tong Cai, Scott H Soderling, Henry H Yin, Mark A Rossi, Haofang E Li, Dongye Lu, Il Hwan Kim, Ryan A Bartholomew, Erin Gaidis, Joseph W Barter, Namsoo Kim, Min Tong Cai, Scott H Soderling, Henry H Yin
Abstract
The contribution of basal ganglia outputs to consummatory behavior remains poorly understood. We recorded from the substantia nigra pars reticulata (SNR), the major basal ganglia output nucleus, during self-initiated drinking in mice. The firing rates of many lateral SNR neurons were time-locked to individual licks. These neurons send GABAergic projections to the deep layers of the orofacial region of the lateral tectum (superior colliculus, SC). Many tectal neurons were also time-locked to licking, but their activity was usually in antiphase with that of SNR neurons, suggesting inhibitory nigrotectal projections. We used optogenetics to selectively activate the GABAergic nigrotectal afferents in the deep layers of the SC. Photo-stimulation of the nigrotectal projections transiently inhibited the activity of the lick-related tectal neurons, disrupted their licking-related oscillatory pattern and suppressed self-initiated drinking. These results demonstrate that GABAergic nigrotectal projections have a crucial role in coordinating drinking behavior.
Figures
References
- Fowler SC, Mortell C. Low doses of haloperidol interfere with rat tongue extensions during licking: a quantitative analysis. Behav Neurosci. 1992;106:386–395.
- Nakamura S, Muramatsu S, Yoshida M. Role of the basal ganglia in manifestation of rhythmical jaw movement in rats. Brain research. 1990;535:335–338.
- Travers JB, Dinardo LA, Karimnamazi H. Motor and premotor mechanisms of licking. Neurosci Biobehav Rev. 1997;21:631–647.
- Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990;13:266–271.
- Yin HH, Ostlund SB, Balleine BW. Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur J Neurosci. 2008;28:1437–1448.
- Takakusaki K, Saitoh K, Harada H, Kashiwayanagi M. Role of basal ganglia-brainstem pathways in the control of motor behaviors. Neuroscience Research. 2004;50:137–151.
- Deniau JM, Chevalier G. The lamellar organization of the rat substantia nigra pars reticulata: distribution of projection neurons. Neuroscience. 1992;46:361–377.
- Beckstead RM. Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes. Neuroscience. 1983;10:767–779.
- Taha EB, Dean P, Redgrave P. Oral behaviour induced by intranigral muscimol is unaffected by haloperidol but abolished by large lesions of superior colliculus. Psychopharmacology (Berl) 1982;77:272–278.
- Redgrave P, Dean P, Donohoe TP, Pope SG. Superior colliculus lesions selectively attenuate apomorphine-induced oral stereotypy: a possible role for the nigrotectal pathway. Brain Res. 1980;196:541–546.
- Wang S, Redgrave P. Microinjections of muscimol into lateral superior colliculus disrupt orienting and oral movements in the formalin model of pain. Neuroscience. 1997;81:967–988.
- Li N, Chen T-W, Guo ZV, Gerfen CR, Svoboda K. A motor cortex circuit for motor planning and movement. Nature. 2015
- Bjursten LM, Norrsell K, Norrsell U. Behavioural repertory of cats without cerebral cortex from infancy. Exp Brain Res. 1976;25:115–130.
- Bignall KE, Schramm L. Behavior of chronically decerebrated kittens. Exp Neurol. 1974;42:519–531.
- Grill HJ. Production and Regulation of Ingestive Consummatory Behavior in the Chronic Decerebrate Rat. Brain Research Bulletin. 1980;5:79–87.
- Rossi MA, Yin HH. Elevated dopamine alters consummatory pattern generation and increases behavioral variability during learning. Front Integr Neurosci. 2015;9:37.
- Spector AC, Klumpp PA, Kaplan JM. Analytical issues in the evaluation of food deprivation and sucrose concentration effects on the microstructure of licking behavior in the rat. Behavioral Neuroscience. 1998;112:678–694.
- Weijnen JA. Licking behavior in the rat: measurement and situational control of licking frequency. Neurosci Biobehav Rev. 1998;22:751–760.
- Gulley JM, Kosobud AE, Rebec GV. Behavior-related modulation of substantia nigra pars reticulata neurons in rats performing a conditioned reinforcement task. Neuroscience. 2002;111:337–349.
- Kim IH, et al. Spine pruning drives antipsychotic-sensitive locomotion via circuit control of striatal dopamine. Nature Neuroscience. 2015;18:883–U326.
- Redgrave P, Marrow L, Dean P. Topographical organization of the nigrotectal projection in rat: evidence for segregated channels. Neuroscience. 1992;50:571–595.
- Chevalier G, Deniau JM, Thierry AM, Feger J. The nigro-tectal pathway. An electrophysiological reinvestigation in the rat. Brain Res. 1981;213:253–263.
- Hikosaka O, Wurtz RH. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol. 1983;49:1285–1301.
- DeLong MR, Crutcher MD, Georgopoulos AP. Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J Neurosci. 1983;3:1599–1606.
- Drager UC, Hubel DH. Topography of visual and somatosensory projections to mouse superior colliculus. J Neurophysiol. 1976;39:91–101.
- Tsumori T, Ono K, Kishi T, Yasui Y. Demonstration of the corticotectobulbar pathway from the orofacial motor cortex to the parvicellular reticular formation in the rat. Brain Res. 1997;755:151–155.
- Komiyama T, et al. Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature. 2010;464:1182–1186.
- Rossi MA, Fan D, Barter JW, Yin HH. Bidirectional modulation of substantia nigra activity by motivational state. PLoS One. 2013;8:e71598.
- Yasui Y, et al. Descending projections from the superior colliculus to the reticular formation around the motor trigeminal nucleus and the parvicellular reticular formation of the medulla oblongata in the rat. Brain Res. 1994;656:420–426.
- Tsumori T, Yasui Y. Organization of the nigro-tecto-bulbar pathway to the parvicellular reticular formation: a light- and electron-microscopic study in the rat. Exp Brain Res. 1997;116:341–350.
- Travers JB, DiNardo LA, Karimnamazi H. Medullary reticular formation activity during ingestion and rejection in the awake rat. Exp Brain Res. 2000;130:78–92.
- Stanek E.t., Cheng S, Takatoh J, Han BX, Wang F. Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination. Elife. 2014;3:e02511.
- Wiesenfeld Z, Halpern BP, Tapper DN. Licking behavior: evidence of hypoglossal oscillator. Science. 1977;196:1122–1124.
- Nakamura Y, Enomoto S, Kato M. The role of medial bulbar reticular neurons in the orbital cortically induced masticatory rhythm in cats. Brain Res. 1980;202:207–212.
- Barter JW, et al. Basal ganglia outputs map instantaneous position coordinates during behavior. Journal of Neuroscience. 2015;35:2703–2716.
- Vong L, et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron. 2011;71:142–154.
- Sparta DR, et al. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat Protoc. 2012;7:12–23.
- Faingold CL, Randall ME. Neurons in the deep layers of superior colliculus play a critical role in the neuronal network for audiogenic seizures: mechanisms for production of wild running behavior. Brain Res. 1999;815:250–258.
- Faingold C, Casebeer D. Modulation of the audiogenic seizure network by noradrenergic and glutamatergic receptors of the deep layers of superior colliculus. Brain Res. 1999;821:392–399.
- Rossi MA, Sukharnikova T, Hayrapetyan VY, Yang L, Yin HH. Operant self-stimulation of dopamine neurons in the substantia nigra. PLoS One. 2013;8:e65799.
- Kato S, et al. A lentiviral strategy for highly efficient retrograde gene transfer by pseudotyping with fusion envelope glycoprotein. Hum Gene Ther. 2011;22:197–206.
- Nelson A, et al. A circuit for motor cortical modulation of auditory cortical activity. J Neurosci. 2013;33:14342–14353.
- Rossi MA, et al. Prefrontal cortical mechanisms underlying delayed alternation in mice. J Neurophysiol. 2012;108:1211–1222.
- Paxinos G, Franklin K. The mouse brain in stereotaxic coordinates. Academic Press; New York: 2003.
Source: PubMed