Fractured Somatotopy in Granule Cell Tactile Areas of Rat Cerebellar Hemispheres Revealed by Micromapping; pp. 94–105

Shambes, Georgia M.; Gibson, John M.; Welker, Wally

doi:10.1159/000123774

Cited by 507 publications

(120 citation statements)

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“…This could imply some processing within the cerebellum, but more research is needed to determine if that occurs. If the cerebellar function implied by our findings depends on the distribution of the several sensory modalities over the cerebellum, we might infer that there is somewhere a complex interaction according to the amount and segregation of the different afferences to the cerebellum (14,15). The effects of cerebellar stimulation at early stations of the somatosensory pathway (16) raise the question of whether the decrease we observed at the thalamus and somatosensory cortex is local or is due to the prior effect at lower sites.…”

Section: Discussionmentioning

confidence: 80%

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

Crispino¹,

Bullock²

1993

How Do Brains Work?

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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...

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Section: Discussionmentioning

confidence: 80%

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

Crispino¹,

Bullock²

1993

How Do Brains Work?

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“…Because the PML region is involved in controlling these movements (18,19) and is metabolically activated as a consequence of such behaviors (20)(21)(22), the FX and VX rats presumably used the existing PML synapses and neurons considerably more than the AC or IC rats did. As a consequence of the extensive physical activity, there was an increase in the density of capillaries in the PML that was not evident in the less active AC and IC rats.…”

Section: Discussionmentioning

confidence: 99%

“…Tactile stimulation of rat forelimbs elicits electrophysiological activity from the PML cortex in a "fractured somatotopy"' type of pattern (19).…”

Section: Methodsmentioning

confidence: 99%

Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats.

Black

Isaacs

Anderson

et al. 1990

Proc. Natl. Acad. Sci. U.S.A.

990

633

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The role of the cerebellar cortex in motor learning was investigated by comparing the paramedian lobule of adult rats given difficult acrobatic training to that of rats that had been given extensive physical exercise or had been inactive. The paramedian lobule is activated during limb movements used in both acrobatic training and physical exercise. Acrobatic animals had greater numbers ofsynapses per Purkin e cell than animals from the exercise or inactive groups. No significant difference in synapse number or size between the exercised and inactive groups was found. This indicates that motor learning required of the acrobatic animals, and not repetitive use of synapses during physical exercise, generates new synapses in cerebellar cortex. In contrast, exercise animals had a greater density ,f blood vessels in the molecular layer than did either the acrobatic or inactive animals, suggesting that increased Synaptic activity elicited compensatory angiogenesis.Although many aspects of experience can alter synaptic connectivity (1-5), it has-been difficult'to relate unequivocally these changes to learning and memory because the morphological effects of leaning could not be isolated from those of behaviors. required to perform the task. For example, maze training (3) and forelimb reach-training (5) can alter neuronal morpholoy, but substantia trepetition of movements is required fo arning these, tasks'. Thus it is not possible to ascrib~e te morphological effects to learning per se.The cerebellar cortex may be particularly appropriate for testing hypotheses about synaptic plasticity because empirical evidence has implicated cerebellar cortex in motor skill learning (6,7,36), and there is some indication that synapse formation underlies cerebellar cortical learning, as suggested by dendritic-field changes in Purkinje cells of rodents and monkeys exposed to challenging. sensory-motor environments (8-10). Synaptogenesis in adult rat cerebellar cortex also occurs when afferents are cut (11,12). Furthermore, theorists have noted the suitability of cerebellar cortex for motor learning, with its convergence of two afferent systems conveying extensive somatic and cerebral state information upon the Purkinje cell, a single-output neuron that modulates motor activity (13)(14)(15)(16)(17).The results of the present study show that learning, as opposed to the motor activity necessary for learning a complex motor task, is responsible for synapse formation in the cerebellar cortex. We report a dissociation oflearning and motor activity, in which animals provided with complex visuomotor learning and minimal motor activity (acrobatic training)-form substantial numbers of new synapses in cerebellar cortex, whereas animals given extensive locomotor exercise with minimal opportunities for learning (repetitive exercise) formed new blood vessels but formed no more new synapses than animals in an inactive control group. MATERIAL AND METHODSAnimals and Training. Thirty-eight adult Long-Evans hooded female rats, kept in small groups...

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“…Finally, the amplification mechanism might provide Purkinje cells with the capacity to detect common features of synaptic input arising from different patterns of granule cell layer activity, which would activate distinct regions of the dendritic tree. Such patterns could, for example, be expected to arise from variations in inputs to the complex fractured maps of the body surface found in the tactile regions of the cerebellum (22,38).…”

mentioning

confidence: 99%

Simulated responses of cerebellar Purkinje cells are independent of the dendritic location of granule cell synaptic inputs.

Schutter

Bower

1994

Proc. Natl. Acad. Sci. U.S.A.

164

128

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Cerebellar Purkh je cell responses to granule cell synaptic inputs were examined with a computer model including active dendritic conductances. Dendritic P-type Ca2+ channels amplified postsynaptic responses when the model was firing at a physiological rate. Small synchronous excitatory inputs applied distally on the large dendritic tree resulted in somatic responses of similar size to those generated by more proximal inputs. In contrast, in a passive model the somatic postsynaptic potentials to distal inputs were 76% smaller. The model predicts that the somatic firing response of Purkinje cells is relatively insensitive to the exact dendritic location of synaptic inputs. We describe a mechanism of Ca2+-mediated synaptic amplification, based on the subspiking threshold recruitment of P-type Ca2+ channels in the dendritic branches surrounding the input site.The interaction between the geometry of a neuron's dendrite and how that neuron processes synaptic information is a central question in neurobiology. Theoretical analysis by Rall (1) and others (2) has shown that in large dendritic trees, synaptic inputs on distal locations will be attenuated much more than inputs on proximal branches before they arrive at the soma. A generally accepted conclusion from these studies is that the exact dendritic location of synaptic inputs is quite important (3). However, this analysis is based on the assumption of a passive dendritic membrane. The cerebellar Purkinje cell has a large dendritic tree (4), covered with an enormous number ofexcitatory parallel fiber synapses (5). The geometry of the cerebellar molecular layer is such that parallel fibers make synapses at similar vertical positions in all Purkinje cells they contact (4 Because increases in membrane conductance also increase the electrotonic length of dendrites, the presence of active channels on the Purkinje cell dendrite and the continuous background synaptic input from the parallel fibers could both be expected to further enhance synaptic attenuation (9-11).In this paper, we use a Purkinje cell model (11,12) to show that the active properties of the dendrite actually interact with the background synaptic input and with the passive electrical properties of the cell to amplify distal synaptic inputs, effectively negating the significance of dendritic location. Our modeling results suggest that in Purkinje cells all granule cell inputs have equal access to the soma independent of their spatial position. If correct, this result has profound implications for the nature of information processing within the cerebellar cortex. MODEL AND METHODSAll simulations used a detailed compartmental model of a Purkinje cell based on reconstructed dendritic anatomy (13). The model was simulated with GENESIS (14) and has been described in detail elsewhere (11,12 The sensitivity of the model to localized synaptic inputs was tested by giving small synchronous excitatory inputs (time to peak, 0.8 ms; 0.7 nS) on 200 spines. These spines were put on dendritic branches with a diamet...

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Fractured Somatotopy in Granule Cell Tactile Areas of Rat Cerebellar Hemispheres Revealed by Micromapping; pp. 94–105

Cited by 507 publications

References 0 publications

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

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

Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats.

Simulated responses of cerebellar Purkinje cells are independent of the dendritic location of granule cell synaptic inputs.

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