Spiking neurons that keep the rhythm

Abstract

Detecting the temporal relationship among events in the environment is a fundamental goal of the brain. Following pulses of rhythmic stimuli, neurons of the retina and cortex produce activity that closely approximates the timing of an omitted pulse. This omitted stimulus response (OSR) is generally interpreted as a transient response to rhythmic input and is thought to form a basis of short-term perceptual memories. Despite its ubiquity across species and experimental protocols, the mechanisms underlying OSRs remain poorly understood. In particular, the highly transient nature of OSRs, typically limited to a single cycle after stimulation, cannot be explained by a simple mechanism that would remain locked to the frequency of stimulation. Here, we describe a set of realistic simulations that capture OSRs over a range of stimulation frequencies matching experimental work. The model does not require an explicit mechanism for learning temporal sequences. Instead, it relies on spike timing-dependent plasticity (STDP), a form of synaptic modification that is sensitive to the timing of pre- and post-synaptic action potentials. In the model, the transient nature of OSRs is attributed to the heterogeneous nature of neural properties and connections, creating intricate forms of activity that are continuously changing over time. Combined with STDP, neural heterogeneity enabled OSRs to complex rhythmic patterns as well as OSRs following a delay period. These results link the response of neurons to rhythmic patterns with the capacity of heterogeneous circuits to produce transient and highly flexible forms of neural activity.

Attractor dynamics in local neuronal networks

“…We now turn to a more detailed model of neuronal activity based on 30,000 integrate-and-fire neurons divided into three distinct populations, resulting in a global connectivity that followed a relay network (Figure 8A, see Materials and Methods) (Thivierge and Cisek, 2008, 2011; Rubinov et al, 2011). Simulated activity in this network (Figure 8B) shows the appearance of a global limit cycle, with two of the populations (in red and blue) exhibiting synchronization with near-zero time-lag (Vicente et al, 2008).…”

“…Synchronized activity may enhance the saliency of incoming stimuli, thus controlling the flow of information transmitted to downstream neurons. Zero-lag synchronization also provides an exquisite mechanism for precise temporal responses to rhythmic stimuli (Thivierge and Cisek, 2008, 2011), and may in itself constitute a unique channel for information transmission. Conceptually, a code based on synchronized action potentials necessitates a fewer number of presynaptic neurons to generate a postsynaptic response, and therefore allows for a greater number of input combinations than a code based on asynchronous activity (Stevens, 1994).…”

A generic deviance detection principle for cortical On/Off responses, omission response, and mismatch negativity

“…Second, the peak amplitude can be larger than the entrained responses during periodic stimuli [33]. Although neural activities that show sustained resonance can be a mechanism underlying the temporal expectancy [57, 99], sustained response alone does not explain the additional delay and higher peak amplitude. How the neural circuits maintain the input periodicity and detect the change is unclear.…”

A generic deviance detection principle for cortical On/Off responses, omission response, and mismatch negativity

“…The OSR differentiates itself from the Off response by its peak latencies that are proportional to the SOA in repetitive stimuli, which reflects the role of temporal expectancy. The models that claim to account for the OSR utilize either an adaptive approach [94] or population coding approach [52] to maintain a short continuation of neural activities (i.e., sustained resonances) that preserve the periodicity of the repetitive stimuli. However, the sustained resonances alone cannot fulfil all observations in terms of peak amplitude and peak latency of the response: (1) For the peak amplitude, the OSR cannot simply rely on the sustained resonance since the amplitude of OSR can be stronger than the evoked response during entrainment [29]; (2) For the peak latency, there should a constant delay upon one more period at the end of the stimuli [2,84], but the sustained resonance rises exactly after one more period at the end of the stimuli.…”

“…(2) The peak amplitude can be larger than the entrained responses during periodic stimuli [29]. Althought neural activities that show sustained resonance can be a mechanism underlying the temporal expectancy [52,94], sustained response alone does not explain the additional delay and higher peak amplitude. How the neural circuits maintain the input periodicity and detect the change is unclear.…”