Elsevier

Brain Research

Volume 768, Issues 1–2, 12 September 1997, Pages 167-176
Brain Research

Research report
Sensory-evoked high-frequency (γ-band) oscillating potentials in somatosensory cortex of the unanesthetized rat

https://doi.org/10.1016/S0006-8993(97)00639-2Get rights and content

Abstract

A 64-channel epipial electrode array was used to investigate high-frequency (γ-band) oscillations in somatosensory cortex of the unanesthetized and unrestrained rat. Oscillations were evoked by manual stimulation of the vibrissae and mystacial pad. Stimulation of the contralateral vibrissae resulted in a significant increase in γ-power during 128-ms epochs taken just following stimulus onset compared to the prestimulus baseline. Stimulation of the ipsilateral vibrissae was completely ineffective in evoking γ-oscillations in any animals. Sensory evoked γ-oscillations were constrained to primary (SI) and secondary (SII) somatosensory cortex. When averaged to an arbitrary reference of peak times in one of the channels, these oscillations exhibited a systematic temporal organization, propagating from the rostral portion of SI to the barrel field proper, and finally to SII. These spatiotemporal characteristics were probably produced by intracortical pathways within rodent somatosensory cortex. The rostrocaudal propagation of γ-oscillations within the barrel field may also reflect whisking patterns observed when the vibrissae are used as a sensory array, suggesting that synchronized γ-oscillations may play a role in assembling punctate afferent information provided by the vibrissae into a coherent representation of a somatosensory stimulus.

Introduction

High-frequency oscillations (20–100 Hz or γ-band) have been observed in field potentials recorded from the cerebral cortex of many species including turtle [32], rat [15], hedgehog [1], rabbit [16], cat 11, 18, 19, and primates 2, 29, 30, 33including man 17, 25, 35. These oscillations result from the synchronized activity of cell populations located primarily in granular cortex. While the frequency content, duration, and focus of individual γ-bursts varies, the spatial distribution of γ-activity is consistently restricted to the cytoarchitectural boundaries defining the cortical regions associated with a given sensory modality 7, 15. Simultaneous multichannel recording in sensory cortex has shown that γ-activity is modality specific, and occurs independently in regions of sensory cortex associated with different sensory modalities [26]. γ- Activity involves both primary and secondary cortical areas of a given sensory modality 7, 15, 26and can engage multiple cortical areas in sensory systems which are thought to perform distributed hierarchical processing [13]. It has been observed bilaterally in homologous hemispheric regions 27, 30with a loss of synchronized activity reported following sectioning of the corpus callosum [12].

Yet, the functional significance of synchronized oscillations in cortical processing is unclear. Although γ-oscillations occur spontaneously, they are often associated with a sensory stimulus or motor task. γ-Activity has been related to vigilance states in humans 17, 25, 35and in the rat [14], suggesting that it may play a role in selective attention. Alternatively, synchronized oscillations may integrate the activity of cell populations processing related information. In the olfactory bulb of the rabbit, oscillatory activity exhibits a spatial distribution that is odorant-related [16]. In visual cortex, synchronized oscillations have been observed within and between cells in cortical columns with similar receptive fields 11, 18, 19. Synchronized activity has also been reported in somatosensory cortex [2], motor and premotor areas [33]and sensorimotor cortex 29, 30of monkeys performing motor tasks. In many cases, synchronization occurs over distances of several millimeters, suggesting a role in temporally coordinating activity within large neural networks.

The somatosensory cortex of the rat exhibits a high degree of anatomical and functional organization which makes it ideal for exploring the possible role of γ-oscillations in neural integration. In contrast to the uniform distribution of cells exhibited by the cortex of most mammals, the facial representation of rodent somatosensory cortex consists of a large collection of cellular aggregates or `barrels' which can be identified using a variety of electrophysiological and histological techniques. Although barrels were known to the early anatomists, the functional significance of the barrel field was first elucidated in the seminal work of Woolsey and Van der Loos [37], who proposed that each barrel is the cortical representation of a single sinus hair. Especially prominent is the representation of the large facial vibrissa which the rodent uses as a sensory array. Collectively, these barrels form a topographic map of the contralateral mystacial pad in which nearest neighbor relationships are preserved, and which processes the punctate sensory information provided by the vibrissae.

We have previously reported results of high resolution mapping of spontaneous and evoked γ-oscillations in somatosensory and auditory cortex of the lightly anesthetized rat using a 64-channel epipial recording array 3, 7, 15, 26, 27. The present results extend these findings to the unanesthetized and unrestrained animal. In preliminary studies, spontaneous potentials from the cortical surface were found to be punctuated by periodic intervals of large-amplitude, high-frequency oscillations in the γ-band, which were most often observed during whisking of the vibrissae, and, moreover, appeared to require contact between the vibrissae and an object in the environment. This anecdotal evidence suggested the need for an experimental paradigm in which the association of γ-oscillations with vibrissae afferents could be investigated in a more controlled fashion. To this end, field potentials recorded at multiple sites over primary and secondary somatosensory cortex were used to quantify the spatial distribution and temporal organization of γ-oscillations which occurred in these regions during manual stimulation of the vibrissae in the quiescent animal. These results characterize oscillatory activity associated with a well-defined sensory stimulus in a system that is highly organized, and whose neuroanatomical structure has been extensively studied.

Section snippets

Surgical procedure

Four adult male Sprague–Dawley rats (450–550 g) were anesthetized to surgical levels using intramuscular injections of ketamine HCl (100 mg/kg) and xylazine (15 mg/kg). A unilateral craniotomy exposed a wide region over parietotemporal cortex in the right hemisphere where the dura was removed. A flat array of 64 silver electrodes configured in an 8×8 matrix (tip diameter, 300 μm; interelectrode distance, 500 μm; total area, 3.5×3.5 mm) was fit with a protective sleeve and positioned over

Results

Fig. 1A depicts the epipial electrode sites (dots) with respect to the vibrissa/barrel field of primary somatosensory cortex (SI) and primary auditory cortex (AI), as determined from CO histology. The relative location of secondary somatosensory cortex (SII) is also indicated, although it is not apparent in CO stained sections. The SEP complex evoked by stimulation of the 25 major contralateral vibrissae had a spatiotemporal pattern that was quite similar across animals (superimposed in Fig. 1

Discussion

These results demonstrate that high-frequency electrical oscillations in the γ-frequency range are a characteristic feature of sensory cortex in the unanesthetized and unrestrained rat. γ-Oscillations occur in somatosensory cortex and are distinctly associated with manual stimulation of the contralateral vibrissae. When stimulus evoked γ-oscillations are averaged, they reveal a highly stereotyped spatiotemporal pattern suggesting an intracortical propagation within the vibrissa/barrel field and

Acknowledgements

This research was supported by United States Public Health Service Grant 1-R01-NS22575, National Science Foundation Grant IBN-9119525, and a Grant in Aid from the Graduate School Council on Research and Creative Work at the University of Colorado at Boulder. The contents of this report are solely the responsibility of the authors and do not necessarily represent the official views of any of the above funding agencies.

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