Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning

Abstract

The temporal relationship between sniffing and the limbic 19 rhythm was studied in rats during odor discrimination reversal learning. The I3 rhythm was monitored as rhythmic slow wave activity (RSA) in the dorsal hippocampal formation, and cyclic nasal airflow (sniffing) was monitored with a thermocouple in the nasal cavity. The training procedures required animals to perform a sequence of whole body locomotion toward one wall of an arena, followed by investigatory sniffing of stimuli through a port while otherwise standing still. Hippocampal RSA was present reliably during the periods of investigatory sniffing. Analyses based on the fast Fourier transform (FFT) demonstrated that this RSA tended to be lower in frequency and amplitude than RSA which occurred during locomotory approach. Other analyses based on the FFT were developed to characterize the nature and parameters of the temporal relationship between rhythmic sniffing and hippocampal RSA as a function of the dominant sniffing frequency during the periods of stimulus sampling. The phase difference between sniffing and RSA tended to vary linearly with frequency so as to maintain a preferred latency relationship between the onset of each sniff cycle and a particular phase of the hippocampal RSA. The phase of RSA to which sniffing was related differed across animals and was correlated with electrode position relative to the phase reversal layers within the hippocampal formation. These results therefore are consistent with the interpretation that, during the periods of stimulus sampling, the sniffs were being timed to maintain a preferred latency relationship with the pacemaker activity which drives the 8 rhythm and the recorded RSA.The consistency with which the animals exhibited the preferred latency relationship varied during the course of training. Across animals, this correlation between sniffing and 8 activity was consistently high during the trials which immediately preceded the achievement of criterion level performance, and the correlation was reduced during the criterion run and/or subsequent trials of overtraining. Thus, the tendency of the animals to exhibit this relationship was not associated specifically with correct performance. Rather, the correlation tended to be highest when the animals were most likely to be evaluating the behavioral relevance of stimuli and were in the process of modifying their responses to those stimuli. The timing of investigatory sniffs as a function of 6' cycle phase may be important for the neural processing of sensory and/or motor information of relevance for response modification.

Theta oscillations and sensorimotor performance

“…This finding is consistent with the necessity for an intact HPC and parahippocampal area for odor-odor associations but not single-odor habituation (23,24). The positive correlation seen here is opposite in sign to the sniffing and HPC theta coherence observed during contingency reversal learning in an earlier study (15). In that study, theta oscillations were coherent with sniffing during early odor contingency reversal learning, with coherence There is no coherence in this band during odor sniffing; although, during other periods, the coherence is high (see Fig.…”

“…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).…”

Rapid and Precise Control of Sniffing During Olfactory Discrimination in Rats

“…Theta oscillations in the hippocampus are subdivided into type 1 or type 2 based on frequency (6 -12 and 4 -6 Hz, respectively) and pharmacological profile (Buzsáki 2002). Both sniffing modes we observed fall within the range of type 1 hippocampal theta and therefore it will be interesting to examine whether both modes could couple to hippocampal oscillations, as previously reported for sniffing during odor sampling (Macrides et al 1982).…”

“…The intrinsic time constants of neural circuits involved in the processing of odor signals in the olfactory bulb and piriform cortex may be tuned to 6-to 9-Hz or theta-band signals (Buonviso et al 2006). 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).…”

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

“…This activity has been studied extensively in the rodent hippocampus (3)(4)(5), but it has also been described in bats (6), cats (7), and, more recently, humans (8)(9)(10)(11). In rodents, theta appears to show close temporal relationships with running (3,12) and sniffing (13), suggesting an association between theta and the rate of sensory input. Although hippocampal theta has been identified in anesthetized monkeys (14), the lack of a clear demonstration of hippocampal theta in awake monkeys has been attributed to the fact that the recording methods typically require immobile, head-affixed monkeys, in contrast to rodent studies using freely moving animals (15).…”