Research report
Attention and arousal related modulation of spontaneous gamma-activity in the auditory cortex of the cat

https://doi.org/10.1016/j.cogbrainres.2003.10.023Get rights and content

Abstract

Sensory information processing in neocortex is associated with rhythmic synchronized gamma frequency firing of sensory cortical units and similar frequency oscillations of the field potentials. Different aspects of the gamma activity (20–80 Hz) have been suggested as correlates of attention, arousal and sensory binding. It is clear that attention has a modality selective influence, while arousal has a more general effect on the sensory systems. We used an experimental conditioning paradigm to separate these differential effects of attention and arousal on spontaneous neocortical gamma activity. We recorded field potentials with epidural electrodes placed above the auditory cortical areas of cats. The animals performed a simple instrumental alimentary conditioning task with different modality (visual and auditory) conditioned stimuli. When they attended to the auditory conditioned stimulus, both frequency and power increase of spontaneous gamma activity were detected. However when they attended visual, we found no power increase of gamma activity recorded above auditory areas, while the frequency increase was the same as in the “attend auditory” condition. We conclude that the power modulation of gamma activity is modality specific and thus can be attributed to selective attention, whereas the frequency modulation of gamma activity shows no modality specificity, it is influenced by the arousal level.

Introduction

Gamma activity refers to high frequency oscillatory processes of the EEG spectrum. Synchronized gamma oscillations have been observed in various species, cortical systems, during behavioral conditions of increased alertness [1], [4], [7], [11], [39], [42], sensory stimulation [10], [13], [15], [24], [33], [36], and cognitive tasks [3], [22], [40], [45], thereby generating considerable interest in their possible function. Sensory information processing in neocortex is associated with rhythmic synchronized gamma frequency firing of sensory cortical units accompanied by similar frequency oscillations of field potentials [8], [16]. Synchronization of gamma-band activities has been implicated with binding of distributed neural activity to a coherent percept, which is indispensable for gestalt type perception [9], [41]. The role of gamma oscillations in plasticity, learning and memory has been emphasized by recent animal and human studies [5], [25], [32], [37], [47].

Changes of gamma activity associated with attention have also been widely studied in various human and animal experiments [4], [6], [12], [14], [17], [31], [38], [42], [46], [49], [51]. These studies suggest that gamma oscillations have a role in the attention-related aspects of sensory processing. Waking arousal related gamma activity changes have also been described in rat and human [21], [23], [27].

In the present study our goal was to separate the effects of selective attention and motivated arousal on spontaneous gamma activity recorded in the auditory cortex of cats. Even though there is no selective attention without arousal, the opposite can be achieved in sensory systems by directing attention towards a different modality.

We taught cats a simple instrumental alimentary conditioning paradigm with two different modality (visual and auditory) conditioned stimuli (CS). Using a given modality CS in an experimental session, the animal's attention was selectively directed towards either auditory or visual modality cues, which yields “attend auditory” and “do not attend auditory” conditions. The spontaneous gamma activity differences in these two cases reflect the effects of selective attention. We recorded spontaneous EEG in three behavioral states: during an indifferent (control) situation and during conditioning which included two different states: when the cats were expecting the CS, and after the CS while the animals waited for the meat reward. These three behavioral states represent different levels of arousal: compared to the quiet state (which is the indifferent situation), the animal actively expecting the CS in the conditioning cage, and after the incentive CS while waiting for the reward is obviously more aroused. The non-modality specific changes of gamma activity during conditioning thus reflect the effects of arousal.

Section snippets

Animals and surgical procedures

The experiments were carried out on four adult cats (four males weighing 3.1–4.2 kg). All procedures were approved by the Institutional Ethical Committee, and carried out in accordance with the SFN policy on the use of animals in neuroscience research.

Brain electrical activity was recorded by chronically implanted epidural electrodes made of 0.23 mm diameter enamel insulated stainless steel wire. They were implanted under pentobarbital anesthesia (40 mg/kg i.p.) using aseptic techniques. Before

Control state

Fig. 2A shows the placement of the epidural electrode matrix in relation to the cat primary and surrounding auditory cortical areas in the right hemisphere (as identified anatomically, see Methods). Our wavelet based gamma burst analysis method revealed two high-energy gamma foci on the auditory cortical areas in the resting cats (Fig. 2B). We recorded the largest gamma activity approximately on the border of area AI and AII (primary focus). This focus had an average gamma burst power of 23956

Discussion

We analyzed the spontaneous auditory cortical field potential changes recorded in different behavioral states in cats with wavelet based time-frequency methods. Our results support the data from earlier studies indicating that spontaneous gamma activity is not a stationary phenomenon, but it consists of isolated gamma bursts [4], [26], [44]. Analyzing the gamma bursts, we identified two high-energy gamma foci over the auditory areas of cats with significantly different dominant frequencies.

Acknowledgements

This research was supported by grants of OTKA F030202 and 32773. We would also like to thank Charles Schroeder and Ankoor Shah for their precious comments.

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