Long-range neural synchrony in behavior

Abstract

Long-range synchrony between distant brain regions accompanies multiple forms of behavior. This review compares and contrasts the methods by which long-range synchrony is evaluated in both humans and model animals. Three examples of behaviorally relevant long-range synchrony are discussed in detail: gamma-frequency synchrony during visual perception, hippocampal-prefrontal synchrony during working memory, and prefrontal-amygdala synchrony during anxiety. Implications for circuit mechanism, translation, and clinical relevance are discussed.

Keywords: coherence; gamma; hippocampus; oscillations; prefrontal cortex; theta.

Figure 1

Structural and dynamic connectivity in the brain. A. Diffusion tensor imaging tractography in the human brain. Reproduced with permission from (Setsompop et al 2013). B. Top, Resting state fMRI image illustrating the correlations observed for a single resting subject between a seed region in the posterior cingulate/precuneus (PCC) and all other voxels in the brain. Warm colors represent positive correlations while cool colors reflect negative correlations. Bottom, An example time course of the PCC (yellow) signal, along with a positively correlated region, the medial prefrontal cortex (mPFC, orange), and a negatively correlated region, the intraparietal sulcus (IPS, blue). Reproduced with permission from (Fox et al 2005). C. Simultaneously recorded local field potentials from depth electrode in the mPFC (top) and ventral hippocampus (vHPC; bottom) in a mouse during active exploration. Raw traces are plotted in gray and theta filtered traces are overlaid in black (adapted with permission from (Adhikari et al 2010)).

Figure 2

Oscillations and synchrony in local field potentials. A. The power spectrum of a local field potential (LFP) recorded from the nucleus accumbens of an actively exploring mouse. The frequency range conventions are color coded below the x-axis (blue: delta, green: theta, yellow: alpha, orange: beta, red: gamma). Right, The raw local field potential is plotted in gray and a band-filtered trace is overlaid to highlight segments with prominent theta (green), delta (blue) and gamma (red) oscillations. B. Top, Two cartoon LFP traces displaying a consistent phase relationship. Bottom, The mPFC and dHPC show peaks in coherence in the delta, theta and gamma frequency range (adapted with permission from Sigurdsson et al 2010). C. Raw (gray) and theta-filtered (blue) mouse mPFC LFP traces, along with simultaneously recorded basolateral amygdala (BLA) single-unit activity illustrating phase locking. Gray bars are aligned on zero phase (reproduced with permission from Stujenske et al 2014). D. Left, schematic of synchronously firing spike trains. Right, cross-correlations of two neurons recorded in middle temporal area of a monkey watching a visual stimulus. The black line outlining the cross-correlogram represents the fitted function used to quantify correlation strength, and the thin black line corresponds to that coherence expected by chance (adapted with permission from (Kreiter & Singer 1996)).

Figure 3

Synchrony deficits in rodent models of schizophrenia predisposition. A. Coherence between LFPs recorded from the hippocampus and medial prefrontal cortex of a mouse model of a microdeletion that raises the risk of schizophrenia by 30-fold (green) and wild-type littermates (gray). Shaded areas are +/− s.e.m. Adapted from Sigurdsson et al., 2010. B. Coherence between hippocampal and medial prefrontal LFPs in a rat model of prenatal infection, a risk factor that raises the risk of schizophrenia by 2–3 fold (gray) and wild-type controls (black). Conventions as in A. Adapted from Dickerson et al., 2010, with permission.