A repetitive intracortical microstimulation pattern induces long-lasting synaptic depression in brain slices of the rat primary somatosensory cortex

Heusler, Peter; Cebulla, Bernhard; Boehmer, Gerd; Dinse, Hubert R.

doi:10.1007/s002210000530

Cited by 27 publications

(20 citation statements)

References 52 publications

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“…The ICMS protocol differs from conventional methods of low-or high-frequency stimulation to induce synaptic plasticity such as long-term potentiation (LTP) or long-term depression (LTD). When we used a slice preparation of adult rat somatosensory cortex, we found that ICMS close to the stimulation site evoked a depression of local field potentials, implying a distinct form of synaptic depression of excitatory mechanisms (32).…”

Section: Discussionmentioning

confidence: 92%

“…The resulting temporally synchronized neuronal discharges are highly effective for the induction of reorganizational processes. ICMS has been used successfully to study rapid, i.e., plastic changes inducible within a few hours in adult motor, somatosensory, and auditory cortex and thalamus; these changes were fully reversible (23)(24)(25)(26)(27)(28)(29)(30)(31)(32). The region of tissue that is stimulated by direct activation during ICMS is very small (50-100 m; refs.…”

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confidence: 99%

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Plasticity of orientation preference maps in the visual cortex of adult cats

Godde

Leonhardt²,

Cords³

et al. 2002

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

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In contrast to the high degree of experience-dependent plasticity usually exhibited by cortical representational maps, a number of experiments performed in visual cortex suggest that the basic layout of orientation preference maps is only barely susceptible to activity-dependent modifications. In fact, most of what we know about activity-dependent plasticity in adults comes from experiments in somatosensory, auditory, or motor cortex. Applying a stimulation protocol that has been proven highly effective in other cortical areas, we demonstrate here that enforced synchronous cortical activity induces major changes of orientation preference maps (OPMs) in adult cats. Combining optical imaging of intrinsic signals and electrophysiological single-cell recordings, we show that a few hours of intracortical microstimulation (ICMS) lead to an enlargement of the cortical representational zone at the ICMS site and an extensive restructuring of the entire OPM layout up to several millimeters away, paralleled by dramatic changes of pinwheel numbers and locations. At the single-cell level, we found that the preferred orientation was shifted toward the orientation of the ICMS site over a region of up to 4 mm. Our results show that manipulating the synchronicity of cortical activity locally without invoking training, attention, or reinforcement, OPMs undergo large-scale reorganization reminiscent of plastic changes observed for nonvisual cortical maps. However, changes were much more widespread and enduring. Such large-scale restructuring of the visual cortical networks indicates a substantial capability for activity-dependent plasticity of adult visual cortex and may provide the basis for cognitive learning processes.

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Section: Discussionmentioning

confidence: 92%

mentioning

confidence: 99%

Plasticity of orientation preference maps in the visual cortex of adult cats

Godde

Leonhardt²,

Cords³

et al. 2002

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

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“…The increase of inhibition adjusts the excitatory output of pyramidal cells and consolidates plasticity during the critical period (Morishita and Hensch, 2008). In a previous study, it was shown that repetitive intracortical microstimulation in brain slices of the rat SI induces long-term depression in the excitatory system (Heusler et al, 2000). As a consequence, the transmitter release of the depressed excitatory synapses is reduced.…”

Section: Suppression Zonementioning

confidence: 99%

Excitation and Inhibition Jointly Regulate Cortical Reorganization in Adult Rats

Benali¹,

Weiler²,

Benali³

et al. 2008

J. Neurosci.

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The primary somatosensory cortex (SI) retains its capability for cortical reorganization after injury or differential use into adulthood. The plastic response of SI cells to peripheral stimulation is characterized by extension of cortical representations accompanied by changes of the receptive field size of neurons. We used intracortical microstimulation that is known to enforce local, intracortical synchronous activity, to induce cortical reorganization and applied immunohistochemical methods in the same individual animals to investigate how plasticity in the cortical topographic maps is linked to changes in the spatial layout of the inhibitory and excitatory neurotransmitter systems. The results reveal a differential spatiotemporal pattern of upregulation and downregulation of specific factors for an excitatory (glutamatergic) and an inhibitory (GABAergic) system, associated with changes of receptive field size and reorganization of the somatotopic map in the rat SI. Predominantly local mechanisms are the specific reduction of the calcium-binding protein parvalbumin in inhibitory neurons and the low expression of the activity marker c-Fos. Reorganization in the hindpaw representation and in the adjacent SI cortical areas (motor cortex and parietal cortex) is accompanied by a major increase of the excitatory transmitter glutamate and c-Fos. The spatial extent of the reorganization appears to be limited by an increase of glutamic acid decarboxylase and the inhibitory transmitter GABA. The local and medium-range net effects are excitatory and can facilitate receptive field enlargements and cortical map expansion. The longer-range increase of inhibition appears suited to limit these effects and to prevent neurons from pathological hyperexcitability.

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“…1B). It has been demonstrated that the early negativity is a pre-synaptic volley, while the late components belong to postsynaptic potentials [38] .…”

Section: Spatial Map Of Neural Circuit In the Hindlimb Represen-mentioning

confidence: 99%

“…However, LTP induced in the neocortex is proven to be related with CS parameter. For example, the optimal form of CS to induce LTP in rat S1 cortex slice is suggested to be high frequency stimulation (HFS), rather than low frequency or theta burst stimulation [38] .…”

Section: Spatial Map Of Neural Circuit In the Hindlimb Represen-mentioning

confidence: 99%

Neural circuits and temporal plasticity in hindlimb representation of rat primary somatosensory cortex: revisited by multi-electrode array on brain slices

Wang

Chang

et al. 2010

Neurosci. Bull.

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Objective The well-established planar multi-electrode array recording technique was used to investigate neural circuits and temporal plasticity in the hindlimb representation of the rat primary somatosensory cortex (S1 area).Methods Freshly dissociated acute brain slices of rats were subject to constant perfusion with oxygenated artificial cerebrospinal fluid (95% O 2 and 5% CO 2 ), and were mounted on a Med64 probe (64 electrodes, 8×8 array) for simultaneous multi-site electrophysiological recordings. Current sources and sinks across all the 64 electrodes were transformed into twodimensional current source density images by bilinear interpolation at each point of the 64 electrodes. Results The local intracortical connection, which is involved in mediation of downward information flow across layers II-VI, was identified by electrical stimulation (ES) at layers II-III. The thalamocortical connection, which is mainly involved in mediation of upward information flow across layers II-IV, was also characterized by ES at layer IV. The thalamocortical afferent projections were likely to make more synaptic contacts with S1 neurons than the intracortical connections did. Moreover, the S1 area was shown to be more easily activated and more intensively innervated by the thalamocortical afferent projections than by the intracortical connections. Finally, bursting conditioning stimulus (CS) applied within layer IV of the S1 area could successfully induce long-term potentiation (LTP) in 5 of the 6 slices (83.3%), while the same CS application at layers II-III induced no LTP in any of the 6 tested slices. Conclusion The rat hindlimb representation of S1 area is likely to have at least 2 patterns of neural circuits on brain slices: one is the intracortical circuit (ICC) formed by interlaminar connections from layers II-III, and the other is the thalamocortical circuit (TCC) mediated by afferent connections from layer IV. Besides, ICC of the S1 area is spatially limited, with less plasticity, while TCC is spatially extensive and exhibits a better plasticity in response to somatosensory afferent stimulation. The present data provide a useful experimental model for further studying microcircuit properties in S1 cortex at the network level in vitro.

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A repetitive intracortical microstimulation pattern induces long-lasting synaptic depression in brain slices of the rat primary somatosensory cortex

Cited by 27 publications

References 52 publications

Plasticity of orientation preference maps in the visual cortex of adult cats

Plasticity of orientation preference maps in the visual cortex of adult cats

Excitation and Inhibition Jointly Regulate Cortical Reorganization in Adult Rats

Neural circuits and temporal plasticity in hindlimb representation of rat primary somatosensory cortex: revisited by multi-electrode array on brain slices

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