Our study provides evidence that individual retinal ganglion cells multiplex two streams of information that the thalamus transmits to cortex. One stream is well known and encodes visual information by changes in firing rate that are time-locked to external visual stimuli. The second channel (which we found by aligning thalamic spikes with respect to the local phase of oscillations in retinal input) encodes information using spike timing relative to intrinsic retinal oscillations (Koepsell and Sommer, 2008
). The amount of extra information in the second channel increases as a function of oscillation strength and can as much as triple the number of bits that each spike carries. Also, because the oscillation-based channel operates in a frequency band separate from that containing the stimulus-locked channel, the contents of both channels could, in principle, be added together in the cortex. Last, these results are easily reproduced by a simple computational model.
How might the oscillation-based channel communicate information to the cortex? To address this question it is useful to consider the physiology and structure of thalamocortical circuits. Coincident thalamic inputs evoke cortical firing more effectively than those spaced several milliseconds apart (Bruno and Sakmann, 2006
; Usrey et al., 1998
). Hence, if relay cells that oscillated in phase were to innervate a common cortical target, their synchronized input could propel oscillations downstream. There is, in fact, evidence for such functional connectivity. Cross-correlation analyses show that a single ganglion cell projects to multiple relay cells which ultimately converge on the same cortical neuron (Hamos et al., 1985
; Usrey et al., 1999
). Therefore, the output of one ganglion cell could drive several relay cells to spike at the same time and provide coincident input to their common target. Further, recordings of local field potentials from the LGN have shown neighboring relay cells oscillate in phase Laufer and Verzeano (1967
). Thus, spikes generated by oscillating relay cells (whether linked to a common ganglion cell or not) are likely to reach cortex simultaneously and sum to generate powerful excitatory drive.
The synchrony that oscillations generate is potentially useful for processing visual images. For instance, computational studies show that retinal oscillations generate synchrony that reduces the occurrence of errors made in encoding of local features (Kenyon et al., 2004
). Oscillations might also contribute to object recognition, as proposed by the “binding by synchrony” hypothesis (Eckhorn et al., 1988
; Gray and Singer, 1989
; Samonds et al., 2006
) by von der Malsburg (1981
). In this scheme, local features in the stimulus are grouped as members of a particular object by phase relationships of visually evoked spikes to intrinsic oscillations. Although this hypothesis was first described for cortex, binding of local receptive fields through synchrony has also been observed in the retina and thalamus (Neuenschwander and Singer, 1996
; Stephens et al., 2006
What information might the second channel encode? It is likely that the oscillation-based channel transmits contextual information about the stimulus. Oscillatory activity in retina is generated by the coordinated activity of distributed networks that span large regions of retinal, and hence visual, space. The idea that oscillations convey contextual information is also supported by recent experiments in frog. Blockade of retinal oscillations abolishes escape behavior elicited by large stimuli that mimic shadows cast by predators but does not impair detection of small objects that resemble prey (Ishikane et al., 2005
). More generally, the oscillation-based channel might serve to convey global information such as the gist of a scene (Navon, 1977
; Torralba, 2003
Having two channels might be better than having one, even if both carried duplicates of the same information. The first copy would be encoded by a familiar mechanism, stimulus-locked changes in spike rate. This low-passed signal would be read out by conventional mechanisms of synaptic integration. To explain how the second copy would be conveyed, we use the analogy of AM radio transmission: here the visual signal modulates the amplitude of the high frequency carrier, in this case the gamma oscillation. Intrinsic cortical oscillations, also in the gamma band, form the band-pass receiver (Fellous et al., 2001
; Hutcheon and Yarom, 2000
; Nowak et al., 1997
); thalamic volleys that arrive near the peaks of the cortical oscillations, when local neurons are most depolarized, would have the best chance of driving activity. The information in the second channel might be read out by the degree of synchrony, or relative phases, of oscillations in the spike trains of converging relay cells. Thus, the visual stimulus is encoded twice, in two separate frequency bands of thalamic spike trains. This redundancy would increase robustness to noise by providing separate alternatives for cortex to decode the spike train, low passing or band passing. Band passing also could provide a mechanism for the selective routing of the oscillation-based channel. Since, the propagation of periodic activity depends on the strength and coherence of pre- and postsynaptic cycles, the amplitude and phase of cortical oscillations would determine when and where the information in the second channels is transmitted. Finally, because the frequency and strength of gamma oscillations in cortex is modulated by attention (Fries et al., 2007
), the contributions of the novel channel might be enhanced during times of heightened vigilance to visual signals.