Abstract
This study demonstrates that gating of responses of the rostral dorsal accessory olive (rDAO) to somatosensory stimulation varies across the estrous hormone cycle of the rat. The rDAO has been suggested as an “error” or event signal generator for the cerebellar cortex. Selective sensory gating of input to this structure may underlie this error signalling function. In the present study, as many as 23 single neurons were recorded simultaneously from either the forepaw or the snout areas of the rDAO. Responses of these neurons to electrical stimulation of peripheral afferents were determined during active movement or non-movement conditions. These results were then compared across the estrous cycle or after administration of the estrous hormones 17 β-estradiol (E2) and/or progesterone (P) to rats on diestrus or following E2 priming. Elevations in circulating estrous hormones produced greater excitatory responses of rDAO neurons to stimulation during non-movement, and, conversely, enhanced inhibition of rDAO activity during active movement of the stimulated peripheral area compared with control diestrous conditions, suggesting that selective gating processes to the rDAO are enhanced by estrous hormones. The results of this study suggest that the night of behavioral estrus is associated with enhanced selective sensory gating processes associated with improved detection and processing of error signals.
Similar content being viewed by others
References
Akaike T (1989) Electrophysiological analysis of the trigeminoolivo-cerebellar (crural and II, lobulus simplex) projection in the rat. Brain Res 482:402–406
Azizi SA, Woodward DJ (1987) Inferior olivary nuclear complex of the rat: morphology and comments on the principles of organization within the olivocerebellar system. J Comp Neurol 263:467–484
Barmack NH, Fagerson M, Fredette BJ, Mugnaini E, Shojaku H (1993) Activity of neurons in the beta nucleus of the inferior olive of the rabiit evoked by natural vestibular stimulation. Exp Brain Res 94:203–215
Bereiter DA, Barker DJ (1984) Hormone-induced enlargement of receptive fields in trigeminal mechanoreceptive neurons. I. Time course, hormone, sex and modality specificity. Brain Res 184:395–410
Berkley KJ, Hand PJ (1978) Projections to the inferior olive of the cat. II. Comparisons of input from the gracile, cuneate and the spinal trigeminal nuclei. J Comp Neurol 180:253–264
Chapin JK, Woodward DJ (1981) Modulation of sensory responsiveness of single somatosensory cortical cells during movement and arousal behaviors. Exp Neurol 72:164–178
Ebner TJ, Bloedel JR (1984) Climbing fiber action on the responsiveness of Purkinje cells to parallel fiber inputs. Brain Res 309:182–186
Gellman R, Houk JC, Gibson AR (1983) Somatosensory properties of the inferior olive of the cat. J Comp Neurol 215:228–243
Gellman R, Gibson AR, Houk JC (1985) Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J Neurophysiol 54:40–60
Havens MD, Rose JD (1988) Estrogen-dependent and estrogen-independent effects of progesterone on the elctrophysiological excitability of dorsal midbrain neurons in golden hamster. Neuroendocrinology 48:120–129
Houk JC, Gibson AR (1987) Sensorimotor processing in the cerebellum. In: King JS (ed) New concepts in cerebellar neurobiology. Liss, New York, pp 387–416
Huerta MF, Hashikawa T, Gayoso MJ, Harting JK (1985) The trigemino-olivary projection in the cat: contributions of individual subnuclei. J Comp Neurol 241:180–190
Kelly MJ, Moss RL, Dudley CA (1977) The effects of microelectrophoretically applied estrogen, cortisol and acetylcholine on medial preoptic septal unit activity throughout the estrous cycle of the female rat. Exp Brian Res 30:53–64
Kow L-M, Pfaff DW (1985) Estrogen effects on neuronal responsiveness to electrical and neurotransmitter stimulation, an in vitro study on the ventromedial nucleus of the hypothalamus. Brain Res 347:1010
Lidierth M, Apps R (1990) Gating in the spino-olivocerebellar pathways to the C1 zone of the cerebellar cortex during locomotion in the cat. J Physiol (Lond) 430:453–469
Llinas R, Baker R, Sotelo C (1973) Electrotonic coupling between neurons in cat inferior olive. J Neurophysiol 37:560–571
Lou JS, Bloedel JR (1992) Responses of sagittally aligned Purkinje cells during perturbed locomotion: synchronous activation of climbing fiber inputs. J Neurophysiol 68:1820–1833
Maekawa K, Simpson JI (1972) Climbing fiber activation of Purkinje cells in the flocculus by impulses transferred through the visual pathway. Brain Res 39:245–251
Majewska MD, Harrison NL, Schwartz RD, Barker JL, Paul SM (1986) Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232:1004–1007
Molinari HH, Dostrovsky JO, el-Yassir N (1990) Functional properties of dorsal horn neurons that project to the dorsal accessory olive. J Neurophysiol 64:1704–1711
Monaghan DT, Yao D, Cotman CW (1984) Distribution of [3H]-AMPA binding sites in rat brain as determined by quantitative autoradiography. Brain Res 324:160–164
Olsen RW, Tobin AJ (1990) Molecular biology of GABAA receptors. FASEB J 4:1469–1480
Simerly RB, Chang C, Muramatsu M, Swanson LW (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76–95
Smith SS (1989a) Estrogen produces long-term increases in excitatory neuronal responses to NMDA and quisqualate. Brain Res 503:354–357
Smith SS (1989b) Progesterone enhances inhibitory responses of cerebellar Purkinje cells mediated by the GABAA receptor subtype. Brain Res Bull 23:317–322
Smith SS, Waterhouse BD, Chapin JK, Woodward DJ (1987a) Progesterone alters GABA and glutamate responsiveness: a possible mechanism for its anxiolytic action. Brain Res 400:353–359
Smith SS, Waterhouse BD, Woodward DJ (1987b) Sex steroid effects on exctrahypothalamic CNS. I. Estrogen augments neuronal responsiveness to iontophoretically applied glutamate in the cerebellum. Brain Res 422:40–51
Smith SS, Chapin JK (1996) Estrous hormones and the olivo-cerebellar circuit. I. Contrast enhancement of sensorimotor-correlated Purkinje cell discharge. Exp Brain Res 111:371–384
Stone LS, Lisberger SG (1986) Detection of tracking errors by visual climbing fiber inputs to monkey cerebellar flocculus during pursuit eye movements. Neurosci Lett 72:163–168
Swenson RS, Sievert CF, Terreberry RR, Neafsey EJ, Castro AJ (1989) Organization of cerebral cortico-olivary projections in the rat. Neurosci Res 7:43–54
Weiss C, Houk JC, Gibson AR (1990) Inhibition of sensory responses of cat inferior olive neurons produced by stimulation of red nucleus. J Neurophysiol 64:1170–1185
Weiss C, Disterhoft JF, Gibson Ar, Houk JC (1993) Receptive fields of single cells from the face zone of the cat rostral dorsal accessory olive. Brain Res 605:207–213
Wong M, Moss RL (1992) Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosci 12:3217–3225
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Smith, S.S., Chapin, J.K. The estrous cycle and the olivo-cerebellar circuit. Exp Brain Res 111, 385–392 (1996). https://doi.org/10.1007/BF00228727
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228727