Human θ Oscillations Related to Sensorimotor Integration and Spatial Learning

Abstract

oscillations in the rat hippocampus have been implicated in sensorimotor integration (Bland, 1986), especially during exploratory and wayfinding behavior. We propose that human cortical activity coordinates sensory information with a motor plan to guide wayfinding behavior to known goal locations. To test this hypothesis, we analyzed invasive recordings from epileptic patients while they performed a spatially immersive, virtual taxi driver task. Consistent with this hypothesis, we found oscillations during both exploratory search and goal-seeking behavior and, in particular, during virtual movement, when sensory information and motor planning were both in flux, compared with periods of self-initiated stillness. oscillations had different topographic and spectral characteristics during searching than during goal-seeking, suggesting that different cortical networks exhibit depending on which cognitive functions are driving behavior (spatial learning during exploration vs orienting to a learned representation during goal-seeking). In contrast, oscillations in the beta band appeared to be related to simple motor planning, likely a variant of the Rolandic mu rhythm. These findings suggest that human cortical oscillations act to coordinate sensory and motor brain activity in various brain regions to facilitate exploratory learning and navigational planning.

Human hippocampal theta power indicates movement onset and distance travelled

“…During navigation, intracranial recordings from depth electrodes in the human hippocampus have shown that theta is more prevalent during movement than during stationary periods (10)(11)(12) and that theta power increases with movement speed (13). In addition, increases in movement-related theta power are seen across the neocortex (10,11,14). These findings support the hypothesis that human theta oscillations might encode self-motion information.…”

“…Hence, this finding strengthens the translational connection between studies of movement-related theta in human and rodent models. Importantly, this increase in theta power around movement onset may have been overlooked by previous human intracranial recording studies that have exclusively compared pure movement and stationary periods that tend to be of short duration (10)(11)(12)14). Theta power increases are not specific to movement-onset periods, however: Both low and high theta power remained above baseline levels during the remainder of movement in the hippocampus and, to a lesser extent, in the lateral temporal lobe.…”

“…Following this response, the object appears in its correct location to provide feedback on their performance in each trial. have compared "pure" movement and stationary periods (10)(11)(12)14). Although theta power is strongest around movement onset, it does not differ statistically from the remainder of movement (P < 0.06) and remains elevated above baseline levels throughout both periods.…”

“…In rodents, theta has been observed in the amygdala during emotional arousal (30, 31) and in pre-and infralimbic cortices during spatial memory tasks (32, 33). In humans, theta oscillations appear to be widespread across the neocortex during navigation in VR environments (10,11,14) as well as during short-and long-term memory tasks (28, 34, 35). We therefore analyzed changes in z-scored theta power between movement periods across patients with depth electrode contacts located in the amygdala (n = 12 patients) and lateral temporal lobe (n = 12 patients; for complementary analysis of n = 8 patients with electrode contacts in all three regions, see Supporting Information).…”

Comparison of spectral analysis methods for characterizing brain oscillations

“…Finally, the P episode method (Caplan et al, , 2003Ekstrom et al, 2005) was designed to measure sustained oscillations, and is used after oscillatory power has been computed by another method (typically wavelets- Fig. 1c,f).…”