Abstract
Typical information processing is thought to depend on the integrity of neurobiological oscillations that may underlie coordination and timing of cells and assemblies within and between structures. The 3–7 Hz bandwidth of hippocampal theta rhythm is associated with cognitive processes essential to learning and depends on the integrity of cholinergic, GABAergic, and glutamatergic forebrain systems. Since several significant psychiatric disorders appear to result from dysfunction of medial temporal lobe (MTL) neurochemical systems, preclinical studies on animal models may be an important step in defining and treating such syndromes. Many studies have shown that the amount of hippocampal theta in the rabbit strongly predicts the acquisition rate of classical eyeblink conditioning and that impairment of this system substantially slows the rate of learning and attainment of asymptotic performance. Our lab has developed a brain–computer interface that makes eyeblink training trials contingent upon the explicit presence or absence of hippocampal theta. The behavioral benefit of theta-contingent training has been demonstrated in both delay and trace forms of the paradigm with a two- to fourfold increase in learning speed over non-theta states. The non-theta behavioral impairment is accompanied by disruption of the amplitude and synchrony of hippocampal local field potentials, multiple-unit excitation, and single-unit response patterns dependent on theta state. Our findings indicate a significant electrophysiological and behavioral impact of the pretrial state of the hippocampus that suggests an important role for this MTL system in associative learning and a significant deleterious impact in the absence of theta. Here, we focus on the impairments in the non-theta state, integrate them into current models of psychiatric disorders, and suggest how improvement in our understanding of neurobiological oscillations is critical for theories and treatment of psychiatric pathology.
Highlights
Recent findings suggest that an estimated 18.1–36.1% of the global population will suffer from a mental disorder, as classified by the Diagnostic and Statistical Manual of Mental Disorders, during their lifetime [1]
Our non-theta state is heterogeneous, with major contributions of delta (0.5–2 Hz) and alpha (8–12 Hz) compared to the homogeneous theta band. This heterogeneity may underlie the detrimental effects seen in our non-theta conditioning. It will be important for future studies to alter the frequencies defined as non-theta, including using individual frequency bands in the denominator, to determine whether the decrease in theta or the heterogeneity of oscillatory bands is responsible for adverse learning
In work by others, triggering trials based on sharp-wave ripple oscillations (150–250 Hz) has been shown to increase eyeblink conditioning (EBC) learning rate and increase the phase locking of theta oscillations to conditioning stimuli [180], suggesting that the heterogeneity of our non-theta state plays an important role
Summary
Recent findings suggest that an estimated 18.1–36.1% of the global population will suffer from a mental disorder, as classified by the Diagnostic and Statistical Manual of Mental Disorders, during their lifetime [1]. Our work has focused on the theta to non-theta [3.5–8 Hz/(0.5–3.5 Hz + 8.5–22 Hz)] ratio, the LabView program can be set with any frequency range in the numerator and denominator. Future studies could utilize the BCI for training contingent on different frequency bands and exploration of different definitions of non-theta.
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