Sub- and suprathreshold adaptation currents have opposite effects on frequency tuning

Key points We provide the first experimental evidence that sub- and suprathreshold adaptation currents, despite having similar effects on spike frequency adaptation, have opposite effects on frequency tuning. Through a combination of computational analysis and mathematical modelling, we reveal how the differential activation properties of these currents can lead to differential effects on the neuronal transfer function. Our findings challenge the common assumption that spike frequency adaptation always attenuates the neural response to low frequency stimuli, and instead suggest that spike frequency adaptation and frequency tuning can be regulated independently of one another. Abstract Natural stimuli are often characterized by statistics that can vary over orders of magnitude. Experiments have shown that sensory neurons continuously adapt their responses to changes in these statistics, thereby optimizing information transmission. However, such adaptation can also alter the neuronal transfer function by attenuating if not eliminating responses to the low frequency components of time varying stimuli, which can create ambiguity in the neural code. We recorded from electrosensory pyramidal neurons before and after pharmacological inactivation of either calcium-activated (IAHP) or KCNQ voltage-gated potassium currents (IM). We found that blocking each current decreased adaptation in a similar fashion but led to opposite changes in the neuronal transfer function. Indeed, blocking IAHP increased while blocking IM instead decreased the response to low temporal frequencies. To understand this surprising result, we built a mathematical model incorporating each channel type. This model predicted that these differential effects could be accounted for by differential activation properties. Our results show that the mechanisms that mediate adaptation can either increase or decrease the response to low frequency stimuli. As such, they suggest that the nervous system resolves ambiguity resulting from adaptation through independent control of adaptation and the neuronal transfer function.