Effects of cholinergic depletion on neural activity in different laminae of the rat barrel cortex

doi:10.1016/S0006-8993(00)02454-9

Brain Research

Volume 872, Issues 1–2, 28 July 2000, Pages 71-76

https://doi.org/10.1016/S0006-8993(00)02454-9 Get rights and content

Abstract

The purpose of these experiments was to determine the effects of cholinergic depletion on spontaneous and evoked activity of neurons in the different layers of the posteromedial barrel subfield (PMBSF) of the rat somatosensory cortex. Acetylcholine neurons in nucleus basalis of Meynert (NBM) were selectively lesioned with an immunotoxin (IT), 192 IgG-saporin. Spontaneous activity was significantly lower in layers II–III, Va, and VI in IT-injected animals compared to control animals. Evoked activity was significantly lower in layers II–III, IV, Vb, and VI of IT-injected animals compared to control animals. The largest difference was observed in layer Vb. Thus, cholinergic depletion causes significant changes in the magnitude of spontaneous and evoked activity but these differences are not completely in register with one another.

Introduction

Acetylcholine (ACh) has been shown to play a vital role in the magnitude of neural activity in the cortex [8], [25], [29], [36]. Nucleus Basalis of Meynert provides the bulk of acetylcholine (ACh) to the cerebral neocortex [3], [17], [19], [23], [26], [32]. The distribution of ACh input from NBM to the cortex is not homogeneous but rather characterized by differentiated laminar inputs [17], [24]. Significantly more ACh fibers are found in layers III and V than in layers I, IV, and VI. The microapplication of ACh has been shown to significantly increase evoked activity in the cortex [22], [27], [28]. Therefore, one purpose of this study was to determine whether cholinergic depletion affects neural activity most in layers that were densely innervated by NBM cholinergic inputs.

Cortical layers are characterized by their unique combinations of cell types, intracortical circuitry, and extrinsic connections. One of the consequences of cholinergic depletion in the cortex is significant slow degeneration of noncholinergic cell bodies and neuropil, particularly of GABAergic neurons and neuropil in layer IV [15], [16]. Since functional properties such as spontaneous and evoked activities, receptive fields, and plasticity in each layer are the integrative results of intracortical circuitry with excitatory and inhibitory inputs [1], [2], [4], [9], [10], [11], [15], [20], [34], [35], [37], [38], these properties are likely to undergo continual change after cholinergic depletion. An additional interest of this study was to determine how spontaneous and evoked activities are affected in different layers of the cortex after 2 weeks of cholinergic depletion.

Section snippets

Procedures and methods

Sixteen Sprague–Dawley albino male rats (2.5 to 3.0 months) were used in this study. Nine and seven animals received intraventricular injections of the immunotoxin (IT) and phosphate buffered saline (PBS), respectively, the vehicle for the IT. Experiments were conducted to minimize discomfort to animals in accordance with the principles of laboratory animal care in NIH publication No. 86–23. Injections of IT and electrophysiological recording procedures were as described in prior publications

Results

The results of these experiments are based on recordings from 351 neurons in control animals and 543 neurons in IT-treated animals. Recordings from these neurons were located in layers II–III, IV, Va, Vb, and VI of the PMBSF cortex (Table 1). All data were obtained from penetrations made through columns of neurons through barrel D2.

Discussion

This study has shown that cholinergic depletion has a significant impact on evoked and spontaneous activities in the PMBSF cortex of rats. Spontaneous activity was significantly reduced in layers II–III, Va, and Vb of IT-injected animals and increased in layer VI of cholinergic depleted animals compared to controls. Evoked activity was significantly decreased in layers II-III, IV, Vb, and VI. Thus, decreased evoked and spontaneous activities are common in some layers following cholinergic

Conclusions

Cholinergic depletion leads to significant decreases in the magnitude of evoked and spontaneous activities in most layers of the PMBSF cortex. The changes in spontaneous and evoked activity in different layers were not congruent. The results are believed to result from progressive changes in the neuropil and neural activity of cholinergic depletion animals.

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Research reportEffects of cholinergic depletion on neural activity in different laminae of the rat barrel cortex

Abstract

Introduction

Section snippets

Procedures and methods

Results

Discussion

Conclusions

Neuroscience

Brain Res.

Internatl. J. Dev. Neurosci.

Brain Res.

Prog. Brain Res.

Neuroscience

Brain Res.

Brain Res.

Spatiotemporal convergence and divergence in the rat S1 ‘barrel’ cortex

J. Comp. Neurol.

Flow of excitation within rat barrel cortex on striking a single vibrissa

J. Neurophysiol.

Topography of cholinergic afferents from nucleus basalis of Meynert to the sensorimotor cortices in the rat

J. Comp. Neurol.

A physiological basis for a theory of synapse modification

Science

192 IgG-saporin: I. Specific lethality for cholinergic neurons in the basal forebrain of the rat

J. Neuropathol. Exp. Neurol.

192 IgG-saporin. 2. Neuropathology in the rat brain

Acta Neuropathol (Berl)

Experience-dependent plasticity in adult rat barrel cortex

Proc. Natl. Acad. Sci. USA

Laminar comparison of somatosensory cortical plasticity

Science

Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons

J. Neurophysiol.

Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex

Nature

Spatial integration and cortical dynamics

Proc. Natl. Acad. Sci. USA

Research report
Effects of cholinergic depletion on neural activity in different laminae of the rat barrel cortex