Synchrony in sensation

Abstract

How neurons encode information has been a hotly debated issue. Ultimately, any code must be relevant to the senders, receivers, and connections between them. This review focuses on the transmission of sensory information through the circuit linking thalamus and cortex, two distant brain regions. Strong feedforward inhibition in the thalamocortical circuit renders cortex highly sensitive to the thalamic synchrony evoked by a sensory stimulus. Neuromodulators and feedback connections may modulate the temporal sensitivity of such circuits and gate the propagation of synchrony into other layers and cortical areas. The prevalence of strong feedforward inhibitory circuits throughout the central nervous system suggests that synchrony codes and timing-sensitive circuits may be widespread, occurring well beyond sensory thalamus and cortex.

Figure 1

Circuits with strong feedforward inhibition (FFI) can selectively gate synchronous over asynchronous inputs. (a) Minimal FFI circuit. (b,c) Integration in circuits without FFI and (d,e) with FFI. Shown are the time courses of input population activity (gray) and, for a single post-synaptic excitatory neuron, the total excitatory conductance received (Gexc, red), total inhibitory conductance (Ginh, blue), and spikes output (black). Spike responses are shown for ten consecutive trials whereas conductances are for a single trial. In both the absence and presence of inhibition synchronous input drives post-synaptic output (b,d), but asynchronous inputs do not produce spiking output in the FFI circuit (e). Adapted from [8] with permission from Springer.

Figure 2

Adaptation enhances discrimination and degrades detection via thalamic synchrony. (a) Detection analyses of how well an ideal observer can classify the presence/absence of a stimulus following either no preceding stimuli (top) or a train of adapting stimuli (bottom). (b) Discrimination analyses of how well an ideal observer could identify which of multiple stimuli were presented with and without adaptation. (c) Comparison of cortical population responses to 5 different stimuli with (bottom) and without (top) adaptation. (d) Thalamic synchrony, measured by the sum of the normalized cross-correlograms of thalamic pairs (insets) over lags ±7.5 ms, decreases with adaptation but to different degrees for each stimulus, diversifying subsequent cortical responses. Colored bars at left, synchrony evoked by 5 different stimulus velocities without preceding stimuli. Colored bars at right, synchrony evoked by same stimulus set after a train of adapting stimuli. Line, synchrony evoked by each pulse in an adapting train (adapting stimulus is similar to s4 and s5). Adapted from [21] with permission from Macmillan Publishers Ltd.

Figure 3

Effects of cholinergic neuromodulation on synaptic connections may alter L4’s sensitivity to synchronous/asynchronous inputs. Acetylcholine increases strength and release probability at TC synapses on L4 excitatory cells via nicotonic receptors (↑) but has no action on TC synapses impinging on L4 inhibitory neurons (X). Strength/release is simultaneously decreased at excitatory and inhibitory intracortical synapses onto excitatory L4 neurons (↓’s). Actions of acetylcholine on synapses contacting inhibitory cells are unknown (?). Effects on intrinsic membrane properties are not illustrated.

Figure 4

The L4-L2/3 circuit may, like the thalamic-L4 circuit, contain a strong disynaptic inhibitory pathway. (a) Excitatory connections from thalamus to L4 neurons are paralleled by excitatory connections from L4 to L2/3 interneurons that in turn can inhibit pyramidal neurons in L2/3. (b) An AP in an L4 spiny neuron (top trace) evokes EPSPs in: (1) L2/3 pyramidal cells at a 2-ms latency and small amplitude and (2) L2/3 interneurons at a 2-ms latency and nearly double the amplitude. Adapted from [45] with permission from the Society for Neuroscience.