Research reportAttention and arousal related modulation of spontaneous gamma-activity in the auditory cortex of the cat
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.
References (51)
- et al.
Changes in power and coherence of brain activity in human sensorimotor cortex during performance of visuomotor tasks
Biosystems
(2001) - et al.
Gamma, alpha, delta, and theta oscillations govern cognitive processes
Int. J. Psychophysiol.
(2001) - et al.
Oscillatory gamma activity in humans: a possible role for object representation
Int. J. Psychophysiol.
(2000) - et al.
Fast fronto-parietal rhythms during combined focused attentive behaviour and immobility in cat: cortical and thalamic localizations
Electroencephalogr. Clin. Neurophysiol.
(1981) - et al.
Anatomical localization of cortical beta rhythms in cat
Neuroscience
(1987) - et al.
Temporal binding and the neural correlates of sensory awareness
Trends Cogn. Sci.
(2001) Spatial properties of an EEG event in the olfactory bulb and cortex
Electroencephalogr. Clin. Neurophysiol.
(1978)- et al.
Spatial direction of attention enhances right hemispheric event-related gamma-band synchronization in humans
Neurosci. Lett.
(2002) - et al.
Selective visual-spatial attention alters induced gamma band responses in the human EEG
Clin. Neurophysiol.
(1999) - et al.
Constant intensity sound stimulation with a bone conductor in the freely moving cat
Electroencephalogr. Clin. Neurophysiol.
(1970)
Effects of emotional arousal in the cerebral hemispheres: a study of oscillatory brain activity and event-related potentials
Clin. Neurophysiol.
An integration of 40 Hz Gamma and phasic arousal: novelty and routinization processing in schizophrenia
Clin. Neurophysiol.
High frequency (gamma-band) oscillating potentials in rat somatosensory and auditory cortex
Brain Res.
High-frequency gamma electroencephalogram activity in association with sleep-wake states and spontaneous behaviors in the rat
Neuroscience
Effects of attention on the reliability of individual neurons in monkey visual cortex
Neuron
Force level modulates human cortical oscillatory activities
Neurosci. Lett.
Modulation of induced gamma band activity in the human EEG by attention and visual information processing
Int. J. Psychophysiol.
Separation of mismatch negativity and the N1 wave in the auditory cortex of the cat: a topographic study
Clin. Neurophysiol.
Oscillatory gamma activity in humans and its role in object representation
Trends Cogn. Sci.
Thalamic modulation of high-frequency oscillating potentials in auditory cortex
Nature
Coupling of beta and gamma activity in corticothalamic system of cats attending to visual stimuli
NeuroReport
Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat
Biol. Cybern.
Modulation of oscillatory neuronal synchronization by selective visual attention
Science
Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection
J. Neurosci.
A 40-Hz auditory potential recorded from the human scalp
Proc. Natl. Acad. Sci. U. S. A.
Cited by (39)
Neural oscillations and speech processing at birth
2023, iScienceUsing convolutional dictionary learning to detect task-related neuromagnetic transients and ageing trends in a large open-access dataset
2023, NeuroImageCitation Excerpt :It is hypothesised that CDL will successfully extract task-related atoms that are biologically plausible, including those that resemble sensorimotor beta and mu transient bursts. This hypothesis is based on the findings of previous literature that demonstrate a functional role of beta and mu transient bursts in sensorimotor tasks (Errington et al., 2020; Feingold et al., 2015; He et al., 2020; Herbert and Lehmann, 1977; Lakatos et al., 2004; Little et al., 2019; Lundqvist et al., 2016; Shin et al., 2017; Wessel, 2020). It is further hypothesised that within task-related atom clusters, atoms will show age-related changes in their spatiotemporal characteristics, in line with previous findings.
Lateralized alpha activity and slow potential shifts over visual cortex track the time course of both endogenous and exogenous orienting of attention
2021, NeuroImageCitation Excerpt :The ACOP was measured between 260 and 360 ms (McDonald et al., 2013), while the LDAP was measured between 500 - 800 ms (Green and McDonald, 2006). For the time frequency analysis, scalp channels were analyzed via complex Morlet wavelets before averaging, following the methods of Lakatos et al. (2004) and Torrence and Compo (1998). Spectral amplitudes were calculated via four-cycle wavelets at 60 different frequencies increasing linearly from 2 to 40 Hz separately for each electrode, time point (every 2 ms), attention condition (left, right), and participant.
Auditory gamma and beta oscillations
2013, Handbook of Clinical NeurophysiologyCitation Excerpt :Distributed gamma band responses were recorded in the cortex, reticular formation, hippocampus and cerebellum of chronically implanted cats (Demiralp et al., 1996). The spontaneous gamma field potentials recorded epidurally from the auditory cortex of cats were enhanced by a simple conditioning task and proved specific for both the sensory modality and topography depending on the arousal level (Lakatos et al., 2004; Jeschke et al., 2008). Spatially distinct gamma rhythms around 35 Hz have been observed in granular layer IV and supragranular layer II/III of the auditory cortex of awake monkeys not involved in tasks (Lakatos et al., 2005); a tonotopic organization has been documented in the awake monkey (Steinschneider et al., 2008).