Abstract
The input/output relationship in primary visual cortex neurons is influenced by the history of the preceding activity. To understand the impact that membrane potential trajectory and firing pattern has on the activation of slow conductances in cortical neurons we compared the afterpotentials that followed responses to different stimuli evoking similar numbers of action potentials. In particular, we compared afterpotentials following the intracellular injection of either square or sinusoidal currents lasting 20 seconds. Both stimuli were intracellular surrogates of different neuronal responses to prolonged visual stimulation. Recordings from 99 neurons in slices of visual cortex revealed that for stimuli evoking an equivalent number of spikes, sinusoidal current injection activated a slow afterhyperpolarization of significantly larger amplitude (8.5±3.3 mV) and duration (33±17 s) than that evoked by a square pulse (6.4±3.7 mV, 28±17 s; p<0.05). Spike frequency adaptation had a faster time course and was larger during plateau (square pulse) than during intermittent (sinusoidal) depolarizations. Similar results were obtained in 17 neurons intracellularly recorded from the visual cortex in vivo. The differences in the afterpotentials evoked with both protocols were abolished by removing calcium from the extracellular medium or by application of the L-type calcium channel blocker nifedipine, suggesting that the activation of a calcium-dependent current is at the base of this afterpotential difference. These findings suggest that not only the spikes, but the membrane potential values and firing patterns evoked by a particular stimulation protocol determine the responses to any subsequent incoming input in a time window that spans for tens of seconds to even minutes.
Highlights
A large number of studies quantifying neuronal sensory responses have been carried out by means of extracellular recordings from anesthetized or awake chronically implanted animals
In order to study the influence of membrane potential trajectory during prolonged stimulation on the subsequent membrane afterpotential, we compared the response evoked by two different protocols: the injection during 20 sec of a square pulse of depolarizing current with that of sinusoidal current at 2 Hz (Fig. 1A)
In order to compare the spike frequency adaptation and the afterpotential evoked by both patterns of discharge, the intensity of the current injection was adjusted such that the total number of evoked action potentials was similar with both protocols
Summary
A large number of studies quantifying neuronal sensory responses have been carried out by means of extracellular recordings from anesthetized or awake chronically implanted animals. Most often the effect of sensory stimulation has been measured by the number, frequency and distribution of action potentials or by input/output relationships; that is, as the suprathreshold evoked response This has strengthened the view that synaptic transmission, passive membrane properties and relatively fast membrane conductances are the main determinants of neuronal integration. Following prolonged neuronal firing (seconds or tens of seconds), a longlasting membrane hyperpolarization and a decrease in neuronal excitability has been attributed to the activation of a Na+dependent K+ current [1,7,8,9,10,11] These long-lasting alterations of the membrane potential and conductance have an impact on the response to subsequent incoming stimuli, such that a given stimulus will evoke a different response depending on the preceding events. We find that the trajectory of the membrane potential during the stimulus and the temporal distribution of action potentials modulate the activation strength of slow afterhyperpolarization and afterdepolarization currents that determine the value of the membrane potential during several seconds after the stimulus
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