Beta- and gamma-frequency coupling between olfactory and motor brain regions prior to skilled, olfactory-driven reaching

Abstract

A major question in neuroscience concerns how widely separated brain regions coordinate their activity to produce unitary cognitive states or motor actions. To investigate this question, we employed multisite, multielectrode recording in rats to study how olfactory and motor circuits are coupled prior to the execution of an olfactory-driven, GO/NO-GO variant of a skilled, rapidly executed (~350-600 ms) reaching task. During task performance, we recorded multi-single units and local field potentials (LFPs) simultaneously from the rats' olfactory cortex (specifically, the posterior piriform cortex) and from cortical and subcortical motor sites (the caudal forepaw M1, and the magnocellular red nucleus, respectively). Analyses on multi-single units across areas revealed an increase in beta-frequency spiking (12-30 Hz) during a ~100 ms window surrounding the Final Sniff of the GO cue before lifting the arm (the "Sniff-GO window") that was seldom seen when animals sniffed the NO-GO cue. Also during the Sniff-GO window, LFPs displayed a striking increase in beta, low-gamma, and high-gamma energy (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) respectively), and oscillations in the high gamma band appeared to be coherent across the recorded sites. These results indicate that transient, multispectral coherence across cortical and subcortical brain sites is part of the coordination process prior to sensory-guided movement initiation.

Cross-correlation of instantaneous amplitudes of field potential oscillations: A straightforward method to estimate the directionality and lag between brain areas

“…For instance, the observations reported here rely on theta-frequency synchrony, which is known to be prominent between the hippocampus and its targets. However, gamma-frequency synchrony can occur across functionally connected cortical regions (Hermer-Vazquez et al, 2007), raising the possibility that the method reported here may be of use in evaluating cortico-cortical functional connectivity if applied to this frequency range. Lastly, in the absence of candidate frequency bands it is possible to apply the amplitude cross-correlation method in successive frequency windows over a broad range, for example, from 1 to 100 Hz.…”

Olfactory system oscillations across phyla

“…Of all the olfactory oscillation bands, beta oscillations are most coherent across areas [55,57–59] and occupy a very narrow frequency band centered about 20 Hz in mammals [60]. We know very little about the mechanisms of olfactory system beta oscillations, except that they require centrifugal input to the OB [39].…”

Rats’ learning of a new motor skill: Insight into the evolution of motor sequence learning

“…The testing apparatus for the skilled task was made of clear Plexiglas with dimensions of 13.1 cm wide × 40 cm deep × 45 cm high (as in Whishaw and Pellis, 1990 and Hermer-Vazquez, 2008; Hermer-Vazquez et al, 2004, 2007a,b). The box stood on a plastic table with clean paper towels covering the floor for each rat.…”

“…For instance, a chimp did not fail to grasp a banana, yet still bring its hand to its mouth and begin chewing. Though it may seem surprising that we would even comment on this, in our extensive experience with rat motor skill and motor sequence learning (Hermer-Vazquez, 2008; Hermer-Vazquez et al, 2004, 2007a,b),we have often seen the animals perform such movements strangely out of order—indeed, including failing to grasp a pellet during a reaching task and yet bringing their reaching paw to their mouths, sometimes with subsequent chewing. Gharbawie, Whishaw and colleagues (Gharbawie et al, 2007; Gharbawie and Whishaw, 2006) have noticed some of the same tendencies of rats learning the same skilled reaching maneuver both before and after cortical injuries.…”

“…Nor has it been demonstrated quantitatively that their learning in other-wise well-studied reach-to-grasp-food task (Gonzalez et al, 2004; Hermer-Vazquez, 2008; Hermer-Vazquez et al, 2004, 2007a,b; Hyland, 1998; Jarratt and Hyland, 1999; Kleim et al, 1998, 2002; Whishaw et al, 2003; Whishaw and Pellis, 1990), or any other type of motor skill, proceeds from sequences of disordered movement primitives to a correctly ordered and smoothened sequence. In primate studies cited above, the more ecologically valid a task appears to be, the more a correct ordering of movement steps is present from initial task learning.…”