Theta oscillations and sensorimotor performance

Abstract

Performance and cognitive effort in humans have recently been related to amplitude and multisite coherence of alpha (7-12 Hz) and theta (4 -7 Hz) band electroencephalogram oscillations. I examined this phenomenon in rats by using theta band oscillations of the local field potential to signify sniffing as a sensorimotor process. Olfactory bulb (OB) theta oscillations are coherent with those in the dorsal hippocampus (HPC) during odor sniffing in a two-odor olfactory discrimination task. Coherence is restricted to the high-frequency theta band (6 -12 Hz) associated with directed sniffing in the OB and type 1 theta in the HPC. Coherence and performance fluctuate on a time scale of several minutes. Coherence magnitude is positively correlated with performance in the two-odor condition but not in extended runs of single odor conditional-stimulus-positive trials. Simultaneous with enhanced OB-HPC theta band coherence during odor sniffing is a significant decrease in lateral entorhinal cortex (EC)-HPC and OB-EC coherence, suggesting that linkage of the olfactory and hippocampal theta rhythms is not through the synaptic relay from OB to HPC in the lateral EC. OB-HPC coupling at the sniffing frequency is proposed as a mechanism underlying olfactory sensorimotor effort as a cognitive process.hippocampus ͉ olfactory bulb ͉ sniffing ͉ behavior ͉ odor discrimination W ithin a given day, performance measures can change, depending on multiple factors. The neural mechanisms that underlie these performance fluctuations in motor and cognitive tasks remain unexplained, with some studies focusing on theta (4-7 Hz in humans and 4-12 Hz in rats) and alpha (7-12 Hz) oscillations as indicators of cognitive effort associated with performance in difficult tasks (1-6).The mammalian hippocampus (HPC) and olfactory bulb (OB) are distinguished by high-amplitude theta oscillations of the local field potential. Hippocampal theta rhythm (4-12 Hz in rats) has been shown to accompany locomotion and cognitive processing, and two theta subbands have been described. High-frequency theta (type 1: 6-12 Hz, atropine-resistant) is linked to locomotion, and low-frequency theta (type 2: 4-6 Hz, atropinesensitive) is seen during immobile states, sensory stimulation, and in urethane-anesthetized animals (7). In the OB, 2-to 12-Hz oscillations have been shown to follow the respiratory cycle with some deviations, and these oscillations are called ''theta'' principally because they occupy a highly overlapping frequency band with hippocampal theta oscillations (8-13).HPC theta oscillations and sniffing have been related to performance and learning in previous studies. Theta oscillatory firing of single interneurons in the HPC has been shown to be related to performance in a cognitively demanding olfactory identification task (14). Hippocampal theta oscillations have also been shown to be coherent with sniffing during the initial stages of odor contingency reversal learning (15) and with OB theta oscillations intermittently during exploratory behavior (16).In th...

Chemical Factors Determine Olfactory System Beta Oscillations in Waking Rats

“…The lead with the best quality signals was chosen from each pair and used for analysis across the entire set of experiments. Quality was assessed for both leads by examining the record for significant movement artifact and line noise, as we have reported previously (Kay 2005). For the OB, the lead with most prominent theta and gamma rhythms was chosen.…”

“…This normalized power was used as the amount of power increase over baseline in further statistical analyses. Coherence analysis was performed for the OB-aPC pair of leads as described previously (Kay 2005;Kay and Freeman 1998). Briefly, the tapered FFTs from all the half-overlapping individual data windows (512 sample windows, ϳ0.25 s) were used to produce averaged auto-and cross-spectra for the odor sampling periods.…”

Rapid and Precise Control of Sniffing During Olfactory Discrimination in Rats

“…In addition, theta oscillations occur not only in olfactory areas but also in the hippocampus, amygdala, striatum, and neocortex and, under some behavioral conditions, sniffing can synchronize with oscillations in different brain areas (Fontanini and Bower 2006;Kay 2005;Macrides et al 1982). Coordination of these oscillations or phase coupling of neuronal populations at preferred frequencies is a mechanism that has been proposed to facilitate sensorimotor integration (Hyman et al 2005;Kay 2005;Kepecs et al 2006;Komisaruk 1977;Siapas et al 2005). Therefore degraded performance at lower respiration frequencies might result from the failure of sniffing to couple properly to central frequencies.…”

“…Respiratory airflow and several other character-istics of sniffing covary with its frequency (Walker et al 1997;Youngentob et al 1987), so high frequencies could enhance olfactory transduction (Hahn et al 1993;Kimbell et al 1997). Alternatively, particular sniffing frequencies within the theta (4-to 12-Hz) range may be favorable for the coordination of olfactory processing with other brain regions (Kay 2005;Kepecs et al 2006;Komisaruk 1977).…”

Decoding signal processing in thalamo-hippocampal circuitry: implications for theories of memory and spatial processing

“…Such mechanisms may involve the neuromodulatory effect of the acetylcholine on thalamic responsiveness (Pare et al, 1987;Pare et al, 1990). The medial septum/diagonal band of Broca complex is the key structure involved in the integration of limbic theta oscillations and somatosensory signals (Kay, 2005;Tsanov et al, 2014b). Septal efferents diverge across several limbic structures, where they regulate the amplitude and frequency of local field theta oscillations as well as neuronal responsiveness.…”