What do single neurons in the rat’s brain contribute to movement and sensation

University College London 2006 (2006) Proc Physiol Soc 3, SA37

Research Symposium: What do single neurons in the rat’s brain contribute to movement and sensation

Michael Brecht1

1. Neuroscience, Erasmus MC, Rotterdam, Netherlands.

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The relationship between action potential (AP) discharge patterns of individual neurons and behavior is a core interest of neurobiology. Extracellular recording and stimulation techniques and have demonstrated that single neuron activity of neurons is closely associated with behavior in mammals, but both techniques are not suited to pinpoint the impact of single neuron activity on behavior. We addressed this issue by assessing effects of single cell stimulation in the vibrissal active touch system of mammals. Specifically we evoked APs in (i) the vibrissal motor cortex of lightly anesthetized rats, (ii) the vibrissal representation of facial nucleus of lightly anesthetized rats, (iii) in the vibrissa / barrel cortex of awake, behaving, head fixed rats. In vibrissa motor cortex we find that AP initiation in individual cells causes long sequences of small and slow multi whisker movements. Intracellular stimulation in layer 5 evokes movements that are phase locked from trial to trial, whereas APs initiated in L6 cells evoke bursts of whisking without specifying the phase of the individual movement. Pyramidal cell and interneuron stimulation evoked movements of opposite directions confirming a functional antagonism of these cell types. AP number had only little effect on whisker movement amplitude but it strongly affected movement latency. AP frequency in contrast did not affect movement latency but determined movement amplitude and direction. In the facial nucleus we find that AP initiation in individual cells causes mainly but not exclusively single whisker movements. Movements are brief and usually fast and each spike causes a very similar fixed latency movement. Thus, motor cortical and facial nucleus cells code movements in very different ways: Cortical APs affect movements on long time scales and APs are read as sequences or “words”, such that the effect (movement latency and direction) of an AP depends on the AP context. In contrast, facial nucleus APs are translated spike by spike to movement twitches. Finally, we investigated sensory effects of single cell stimulation in barrel cortex. To this end we electrically stimulated single neurons in primary somatosensory cortex of awake, behaving, head fixed rats. Animals were first trained to report trains of microstimulation pulses of the barrel cortex by breaking an infrared beam with the tongue. The animal’s detection threshold for microstimulation decreased over a period of a few days to currents of 2-7 µA. Once the animal had reached asymptotic performance, microstimulation trials were randomly mixed with trials in which we evoked 5-40 action potentials (APs) in single cortical neurons using juxtacellular stimulation in the nA range. We found that animals responded significantly more often to single-cell stimulation than to randomly intermixed control trials. Results varied from cell to cell and the average size of the effect was modest: the average single-cell hit rate was 25.8% compared to a control hit rate of 19.9% (an increase of 30%). Additional control experiments showed that this sensory bias was dependent on the generation of APs by juxtacellular stimulation. Thus, subthreshold juxtacellular stimulation or injection of twice the stimulation current into the extracellular space did not affect the animal’s behavior. The occurrences of sensory biases covaried with the animal’s performance in the microstimulation task, as single-cell stimulation trials flanked by misses on microstimulation trials were not different from control trials. We conclude: (i) the activity of individual neurons can affect behavior, (ii) single cell stimulation is a most powerful tool to decode the meaning spike trains, (iii) the capacity of an individual neuron to evoke behaviors is most astonishing given the large number of neurons in the rat brain. Thus, sparse AP activity may suffice control behavior and APs can be translated into action with the utmost precision.



Where applicable, experiments conform with Society ethical requirements.

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