Retinal oscillations carry visual information to cortex

Abstract

Thalamic relay cells fire action potentials that transmit information from retina to cortex. The amount of information that spike trains encode is usually estimated from the precision of spike timing with respect to the stimulus. Sensory input, however, is only one factor that influences neural activity. For example, intrinsic dynamics, such as oscillations of networks of neurons, also modulate firing pattern. Here, we asked if retinal oscillations might help to convey information to neurons downstream. Specifically, we made whole-cell recordings from relay cells to reveal retinal inputs (EPSPs) and thalamic outputs (spikes) and then analyzed these events with information theory. Our results show that thalamic spike trains operate as two multiplexed channels. One channel, which occupies a low frequency band (<30 Hz), is encoded by average firing rate with respect to the stimulus and carries information about local changes in the visual field over time. The other operates in the gamma frequency band (40–80 Hz) and is encoded by spike timing relative to retinal oscillations. At times, the second channel conveyed even more information than the first. Because retinal oscillations involve extensive networks of ganglion cells, it is likely that the second channel transmits information about global features of the visual scene.

Oscillations, Phase-of-Firing Coding, and Spike Timing-Dependent Plasticity: An Efficient Learning Scheme

“…However evidence for it is still scarce in the cortex. For example, Montemurro et al (2008), Ray et al (2008), and Kayser et al (2009) all looked for it unsuccessfully [but see König et al (1995), Fries et al (2001), Hoffman et al (2009), andKoepsell et al (2009) for exceptions]. In the studies by Jacobs et al (2007) and Ray et al (2008), some spikes did lock to gamma oscillations, but the preferred phases always tended to be near the oscillation peaks, ruling out PoFC, but suggesting instead a binary code in which information would be coded in the combination of neurons which fire at least once in each oscillation cycle.…”

Modulation of Fast Narrowband Oscillations in the Mouse Retina and dLGN According to Background Light Intensity

“…Based on our work, it seems probable that that phenomenon was a reflection of narrowband oscillations, and, as originally proposed (Barlow and Levick, 1969), such regularization could improve signal-to-noise ratio (SNR) at the single-unit level. Indeed, more recently it was shown that phase locking of dLGN spikes to retinal oscillations can significantly enhance the information rate (Koepsell et al, 2009).…”

“…In the early visual system, these oscillations have been recorded in the retina, dorsal lateral geniculate nucleus (dLGN), and primary visual cortex (Castelo-Branco et al, 1998). They are thought to provide a substrate for inter-area communication (Fries, 2005) and visual coding (Gray et al, 1989;Koepsell et al, 2009), and given the well-known association between irradiance and visual performance, understanding the impact of irradiance on these narrowband oscillation has obvious importance. Nonetheless, studies of narrowband oscillations in the early visual system have heretofore concentrated on the effects of spatially structured patterns at single-light backgrounds.…”

Sensory Input Drives Multiple Intracellular Information Streams in Somatosensory Cortex

“…For example, in the visual thalamus, spike timing relative to the stimulus (Ͻ30 Hz) carries information about local changes in the visual field, whereas timing relative to retinal oscillations (40 -80 Hz) appears to provide contextual information about global properties of the scene (Koepsell et al, 2009).…”

“…This implies a general principle for information multiplexing: that spike timing locked to activity fluctuations, and not just to the stimulus, is also capable of encoding information (Ahissar and Vaadia, 1990;O'Keefe and Recce, 1993;Hopfield, 1995;Friedrich et al, 2004;Lisman, 2005;Fries et al, 2007;Koepsell et al, 2009Koepsell et al, , 2010Nadasdy, 2009;Panzeri et al, 2010). To evaluate whether, similarly, additional information can be gained by considering the membrane potential of a cortical neuron each time it fires a spike, we labeled each spike with the membrane potential phase at the time of firing, computed from the 20 Hz low-pass filtered signal (binned into N R ϭ 4 uniformly spaced values, i.e., quadrants).…”