Distinguishing Neural Adaptation and Predictive Coding Hypotheses in Auditory Change Detection.

The auditory mismatch negativity (MMN) component of event-related potentials (ERPs) has served as a neural index of auditory change detection. MMN is elicited by presentation of infrequent (deviant) sounds randomly interspersed among frequent (standard) sounds. Deviants elicit a larger negative deflection in the ERP waveform compared to the standard. There is considerable debate as to whether the neural mechanism of this change detection response is due to release from neural adaptation (neural adaptation hypothesis) or from a prediction error signal (predictive coding hypothesis). Previous studies have not been able to distinguish between these explanations because paradigms typically confound the two. The current study disambiguated effects of stimulus-specific adaptation from expectation violation using a unique stimulus design that compared expectation violation responses that did and did not involve stimulus change. The expectation violation response without the stimulus change differed in timing, scalp distribution, and attentional modulation from the more typical MMN response. There is insufficient evidence from the current study to suggest that the negative deflection elicited by the expectation violation alone includes the MMN. Thus, we offer a novel hypothesis that the expectation violation response reflects a fundamentally different neural substrate than that attributed to the canonical MMN.

Stimulus-evoked modulation of sensorimotor pyramidal neuron EPSPs.

Sensory cortical neurons display substantial receptive field dynamics during and after persistent sensory drive. Because a cell's response properties are determined by the inputs it receives, receptive field dynamics are likely to involve changes in the relative efficacy of different inputs to the cell. To test this hypothesis, we have investigated if brief repetitive stimulus drive in vitro alters the efficacy of two types of corticocortical inputs to layer V pyramidal cells. Specifically, we have used whole cell recordings to measure the effect of repetitive electrical stimulation at the layer VI/white matter (WM) border on the synaptic response of layer V pyramidal cells to corticocortical input evoked by electrical stimulation of layer I or layer II/III and emulated by local application of glutamate. Repetitive stimulation (10 Hz for 3 s) at the layer VI/WM border transiently potentiated excitatory postsynaptic potentials (EPSPs) evoked by electrical stimulation of layer II/III by 97 +/- 12% (mean +/- SE). The recovery of EPSP amplitude to its preconditioning value was well-described by a single-term decaying exponential with a time constant of 7.2 s. The same layer VI/WM conditioning train that evoked layer II/III EPSP potentiation frequently caused an attenuation of layer I EPSPs. Similarly, subthreshold postsynaptic responses to local glutamate application in layers II/III and I were potentiated and attenuated, respectively, by the conditioning stimulus. Potentiation and attenuation could be evoked in the same cell by repositioning the glutamate puffer pipette in the appropriate layer. The conditioning stimulus that led to the transient modification of upper layer EPSP efficacy also evoked a slow depolarization in glial cells. The membrane potential of glial cells recovered with a time course similar to the dissipation of the potentiation effect, suggesting that stimulus-evoked changes in extracellular potassium (ECK) play a role in layer II/III EPSP potentiation. Consistent with this proposal, increasing the bath concentration of ECK caused a substantial increase of layer II/III EPSP amplitude. EPSP potentiation was sensitive to postsynaptic membrane potential and, more importantly, was significantly weaker for synaptic currents than for synaptic potentials, suggesting that it involves the recruitment of a postsynaptic voltage-dependent mechanism. Two observations suggest that layer II/III EPSP potentiation may involve the recruitment of postsynaptic sodium channels: EPSP potentiation was strongly reduced by intracellular application of N-(2,6-dimethyl-phenylcarbamoylmethyl) triethylammonium bromide (QX-314) and responses to local glutamate application were potentiated by high ECK in the presence of cadmium but not in the presence of tetrodotoxin. The results demonstrate a novel way in which brief periods of repetitive stimulus drive are accompanied by rapid, transient, and specific alterations in the functional connectivity and information processing characteristics of sensorimotor cortex.