Reverse physiology in the sensory system

Arthur Houweling, Birgit Voigt, Michael Brecht

How do action potentials in single sensory cortical neurons relate to perception? Classical recording approaches have successfully described how neurons respond to sensory stimuli, but they do not tell us how the brain reads out these responses. To establish causal links between single-cell activity and perception one would like to employ a reverse physiology approach, in which one analyzes behavioral responses to cellular activity (rather than cellular responses as in classical physiology).

Using such an approach we have recently shown that stimulation of single neurons in rat somatosensory cortex affects behavioral responses in a detection task. We trained animals to respond to microstimulation of barrel somatosensory cortex. We then initiated short trains of action potentials in single neurons by juxtacellular stimulation. Animals responded significantly more often in single-cell stimulation trials than in catch trials without stimulation. These results demonstrate that single neuron activity can cause sensations, suggesting that cortical sensory representations are much sparser than previously anticipated. In further studies it should be possible to establish how the frequency and number of action potentials are related to the evoked sensations.



Figure legend: Behavioral responses to stimulation of a single layer 5b pyramidal neuron.  
(a) Reconstruction of the stimulated neuron with dendritic tree (red) and axon (blue, incompletely filled). Superimposed is a micrograph of a stimulation pipette and a tungsten microstimulation electrode aligned along the electrode track. Barrel rows (brown) are labelled with letters.
L = layer, WM = white matter.
(b) Action potential raster plots (ticks) and first lick responses (red squares) during juxtacellular single cell stimulation trials (top), no-current-injection catch trials (middle) and 19 randomly selected microstimulation trials (bottom).
(from Houweling and Brecht, Nature 451: 65-68, 2008)

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