Cerebellum mediates modality-specific modulation of sensory responses of midbrain and forebrain in rat

Abstract

Evidence of a sensory role of the cerebellum, mediating a modulation of effectiveness of afferent input at other parts of the brain, has been reported previously for certain sense modalities but has not been evaluated across several in a mammal. After a conditioning train of stimuli applied to the cerebellar surface in unanesthetized rats, diffuse flashes, acoustic clicks, and shocks to the sciatic nerve evoked multiunit and field potential responses that were recorded at three levels: midbrain, thalamus, and cerebral cortex. At a best interval between end of conditioning train (cerebellar) and test (sensory) stimuli, all three levels show modulation of the evoked responses, each in a specific direction (enhancement or depression), with a characteristic time course. Visual responses in the tectum are enhanced; those in the cortex are depressed. Tectal responses that have been nearly abolished by increasing background illumination are partially restored by the conditioning cerebellar train. Auditory brainstem responses (short latency, <10 ms, far-field waves I to HI, attributed to medullary levels) are depressed; wave IV from the inferior colliculus is relatively enhanced at short intervals and is depressed at longer intervals. Somatosensory responses in thalamus and cortex are depressed. Lobulae V, VI, and VII of the vermis are more effective sites of stimulation than other areas tested. Most of the modulations are ascribed to central sites; a few are ascribed to peripheral sites.In spite of some indications that the cerebellum plays a role in modulating sensory input, such a function is seldom mentioned in treatments of cerebellar physiology; this is in line with the prevailing emphasis on its motor functions. Boone et al. (1) reported that cerebellar stimulation can depress visual evoked potentials of the cerebral cortex and lateral geniculate body. Wolfe and Kos (2) found that lesions of the cerebellum apparently disinhibit auditory input. Velluti and Crispino (3) showed that stimulation of the cerebellum depresses the cochlear microphonic and auditory nerve response and cooling enhances it; these authors proposed a tonic influence of the cerebellum by way of the olivocochlear bundle. Looking for the phylogenetic generality of this influence, Crispino (4) found evidence of cerebellar modulation in the catfish upon several afferent modalities, some being depressed and others enhanced by cerebellar activation, as well as evidence that the influence is not only on peripheral sensory sites but also on central sites.The question here addressed is whether in mammals there is an influence of the cerebellum upon central afferent systems of several modalities. We looked for direct action on brainstem as well as higher levels, in visual, auditory, and somatosensory modalities, in the rat. We report that some levels and modalities are consistently depressed and others are enhanced, each with characteristic dynamics. MATERIALS AND METHODSPreparation. The experiments were made on 22 female albino rats weighing a...

Prediction and preparation, fundamental functions of the cerebellum.

“…Such effects have been documented for visual, auditory, somatosensory, and nociceptive stimuli (e.g., Newman and Reza 1979;Crispino and Bullock 1984;Liu et al 1993). For example,…”

“…This tremendous number of neurons, coupled with the high input-to-output axon ratio (cerebellar afferents to efferents are 40:1; Carpenter 1991) suggests that its function must be massively integrative. It is also one of the most widely connected structures, having physiological connections with all major divisions of the CNS (Moruzzi and Magoun 1949;Snider 1950Snider , 1967Bava et al 1966;Sasaki et al 1972Sasaki et al , 1979Kitano et al 1976;Watson 1978;Itoh and Mizuno 1979;Newman and Reza 1979;Saint-Cyr and Woodward 1980a,b;Vilensky and Van Hoesen 1981;Crispino and Bullock 1984;Ito 1984;Haines and Dietrichs 1987;King 1987;Nieuwenhuys et al 1988;Schmahmann and Pandya 1989;Ghez 1991;Ikai et al 1992;Llimis and Sotelo 1992;Thielert and Thier 1993;Glickstein et al 1994;Lynch et al 1994;Middleton andStrick 1994, Schmahmann 1996). Moreover, experimental data and, in particular, the results of recent fMR imaging and PET studies, indicate that the cerebellum might be involved in a wide range of functions, including attention, associative learning, practice-related learning, procedural learning, declarative memory, working memory, semantic association, conditioned anxiety, mental exploration, and complex reasoning and problem solving as well as sensory, motor and motor skill acquisition (see Table 1).…”

Light Stimulus Frequency Dependence of Activity in the Rat Visual System as Studied With High-Resolution BOLD fMRI

“…Although both cortex and superior colliculus are known to project to the flocculus-paraflocculus, another pathway exists from the superior colliculus to other areas in the cerebellum, such as the vermal lobules VI and VII, which are involved in eye-head movements during saccades (Akaike 1985;Burne and Woodward 1984). Crispino (Crispino and Bullock 1984) demonstrated that responses recorded at the surface of the superior colliculus evoked by bilateral flashes were augmented by cerebellar stimulation of the dorsal vermis (lobules V-VII). In this respect, observed correlations could confirm this closer relationship between the floccular complex and the visual cortex rather than between either of these structures and the superior colliculus.…”

Detecting violations of sensory expectancies following cerebellar degeneration: A mismatch negativity study

“…In contrast, the primary sensory cortex was only activated after actually delivered stimuli and showed no response to the unexpected omissions. Further support for the sensory prediction hypothesis comes from electrophysiological experiments in non-humans showing that electrical stimulation of the cerebellum modulates sensory responses in extracerebellar regions (e.g., superior colliculus, thalamus) to a range of stimuli (Crispino & Bullock, 1984).…”