Rats' learning of a new motor skill: insight into the evolution of motor sequence learning.

Recent behavioral and neural evidence has suggested that ethologically relevant sub-movements (movement primitives) are used by primates for more complex motor skill learning. These primitives include extending the hand, grasping an object, and holding food while moving it toward the mouth. In prior experiments with rats performing a reach-to-grasp-food task, we observed that especially during early task learning, rats appeared to have movement primitives similar to those seen in primates. Unlike primates, however, during task learning the rats performed these sub-movements in a disordered manner not seen in humans or macaques, e.g. with the rat chewing before placing the food pellet in its mouth. Here, in two experiments, we tested the hypothesis that for rats, learning this ecologically relevant skill involved learning to concatenate the sub-movements in the correct order. The results confirmed our initial observations, and suggested that several aspects of forepaw/hand use, taken for granted in primate studies, must be learned by rats to perform a logically connected and seemingly ecologically important series of sub-movements. We discuss our results from a comparative and evolutionary perspective.

A putatively novel form of spontaneous coordination in neural activity.

We simultaneously recorded local field potentials from three sites along the olfactory-entorhinal axis in rats lightly anesthetized with isoflurane, as part of another experiment. While analyzing the initial data from that experiment with spectrograms, we discovered a potentially novel form of correlated neural activity, with near-simultaneous occurrence across the three widely separated brain sites. After validating their existence further, we named these events Synchronous Frequency Bursts (SFBs). Here we report our initial investigations into their properties and their potential functional significance. In Experiment 1, we found that SFBs have highly regular properties, consisting of brief (approximately 250 ms), high amplitude bursts of LFP energy spanning frequency ranges from the delta band (1-4 Hz) to at least the low gamma band (30-50 Hz). SFBs occurred almost simultaneously across recording sites, usually with onsets <25 ms apart, and there was no clear pattern of temporal leading or lagging among the sites. While the SFBs had fairly typical, exponentially decaying power spectral density plots, their coherence structure was unusual, with high peaks in several narrow frequency ranges and little coherence in other bands. In Experiment 2, we found that SFBs occurred far more often under light anesthesia than deeper anesthetic states, and were especially prevalent as the animals regained consciousness. Finally, in Experiment 3 we showed that SFBs occur simultaneously at a significant rate across brain sites from putatively different functional subsystems--olfactory versus motor pathways. We suggest that SFBs do not carry information per se, but rather, play a role in coordinating activity in different frequency bands, potentially brain-wide, as animals progress from sleep or anesthesia toward full consciousness.

Tracing 'driver' versus 'modulator' information flow throughout large-scale, task-related neural circuitry.

PRIMARY OBJECTIVE: To determine the relative uses of neural action potential ('spike') data versus local field potentials (LFPs) for modeling information flow through complex brain networks. HYPOTHESIS: The common use of LFP data, which are continuous and therefore more mathematically suited for spectral information-flow modeling techniques such as Granger causality analysis, can lead to spurious inferences about whether a given brain area 'drives' the spiking in a downstream area. EXPERIMENT: We recorded spikes and LFPs from the forelimb motor cortex (M1) and the magnocellular red nucleus (mRN), which receives axon collaterals from M1 projection cells onto its distal dendrites, but not onto its perisomatic regions, as rats performed a skilled reaching task. RESULTS AND IMPLICATIONS: As predicted, Granger causality analysis on the LFPs-which are mainly composed of vector-summed dendritic currents-produced results that if conventionally interpreted would suggest that the M1 cells drove spike firing in the mRN, whereas analyses of spiking in the two recorded regions revealed no significant correlations. These results suggest that mathematical models of information flow should treat the sampled dendritic activity as more likely to reflect intrinsic dendritic and input-related processing in neural networks, whereas spikes are more likely to provide information about the output of neural network processing.

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

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 (approximately 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 approximately 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 (12-30, 30-50, and 50-100 Hz, 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.

The reach-to-grasp-food task for rats: a rare case of modularity in animal behavior?

Humans and non-human animals make use of sensory hierarchies in "selecting" strategies for solving many cognitive and behavioral tasks. Often, if a preferred type of sensory information is unavailable or is not useful for solving a given task, the animal can switch to a lower-priority strategy, making use of a different class of sensory information. In the case of rats performing a classic reach-to-grasp-food task, however, prior studies indicate that the reaching maneuver may be a fixed action pattern that is guided exclusively by the food's odor plume until the point of contact with the food morsel [Whishaw IQ, Tomie JA. Olfaction directs skilled forelimb reaching in the rat. Behav Brain Res 1989;32(1):11-21; Metz GA, Whishaw IQ. Skilled reaching an action pattern: stability in rat (Rattus norvegicus) grasping movements as a function of changing food pellet size. Behav Brain Res 2000;116(2):111-22; Whishaw IQ. Did a change in sensory control of skilled movements stimulate the evolution of the primate frontal cortex? Behav Brain Res 2003;146(1/2):31-41]. We sought to confirm and extend these findings in several ways. In Experiment 1, using a GO/NO-GO variant of the classic task, we demonstrated that rats used the GO target's odor both to trigger and guide their reaches. In Experiment 2, we showed that rats deprived of (a) vision, (b) object-recognizing rostral whiskers and forearm sinus hairs, or (c) both, displayed no deficits in triggering and guiding their reaches. Finally, in a third experiment in which the GO target's location varied randomly across trials and only olfactory cues were available, we demonstrated that rats could determine the spatial endpoint of their reach without any loss of accuracy. Combined with results from a prior study in which bulbectomized rats never developed a new, successful reaching strategy despite extensive post-operative training [Whishaw IQ, Tomie JA. Olfaction directs skilled forelimb reaching in the rat. Behav Brain Res 1989;32(1):11-21], these results indicate that rats do not have a sensory hierarchy for solving the reach-to-grasp-food task, but rather, are guided by olfaction alone until their paw contacts the food morsel.

Rapid learning and flexible memory in "habit" tasks in rats trained with brain stimulation reward.

Two groups of rats, one rewarded with sweetened food and the other rewarded with medial forebrain bundle (MFB) stimulation, were trained to home in on and dig for a buried object coated with a target odor. After each group had 15 training trials, MFB rats searched with greater accuracy and speed than food-rewarded rats. MFB rats were subsequently tested (1) after 6 weeks with no additional practice; (2) with food or non-food distractor odors, and (3) with major spatial alterations to the search environment, and in all cases searched with the same high accuracy, short search time, and low level of distractibility as in baseline. These results suggest that the high motivation provided by MFB reward engenders rapidly formed, long-lasting, and surprisingly flexibly deployable "habit" memories.