Changes in the sensory environment are good indicators for behaviorally relevant events and strong triggers for the reallocation of attention. In the auditory domain, violations of a pattern of repetitive stimuli precipitate in the event-related potentials as mismatch negativity (MMN). Stimulus-specific adaptation (SSA) of single neurons in the auditory cortex has been proposed to be the cellular substrate of MMN (Nelken and Ulanovsky, 2007). However, until now, the existence of SSA in the awake auditory cortex has not been shown. In the present study, we recorded single and multiunits in parallel with evoked local field potentials (eLFPs) in the primary auditory cortex of the awake rat. Both neurons and eLFPs in the awake animal adapted in a stimulus-specific manner, and SSA was controlled by stimulus probability and frequency separation. SSA of isolated units was significant during the first stimulus-evoked "on" response but not in the following inhibition and rebound of activity. The eLFPs exhibited SSA in the first negative deflection and, to a lesser degree, in a slower positive deflection but no MMN. Spike adaptation correlated closely with adaptation of the fast negative deflection but not the positive deflection. Therefore, we conclude that single neurons in the auditory cortex of the awake rat adapt in a stimulus-specific manner and contribute to corresponding changes in eLFP but do not generate a late deviant response component directly equivalent to the human MMN. Nevertheless, the described effect may reflect a certain part of the process needed for sound discrimination.

The detection of novel and therefore potentially behavioral relevant stimuli is of fundamental importance for animals. In the auditory system, stimulus-specific adaptation (SSA) resulting in stronger responses to rare compared with frequent stimuli was proposed as such a novelty detection mechanism. SSA is a now well established phenomenon found at different levels along the mammalian auditory pathway. It depends on various stimulus features, such as deviant probability, and may be an essential mechanism underlying perception of changes in sound statistics. We recorded neuronal responses from the ventral part of the medial geniculate body (vMGB) in Mongolian gerbils to determine details of the adaptation process that might indicate underlying neuronal mechanisms. Neurons in the vMGB exhibited a median spike rate change of 15.4% attributable to a fast habituation to the frequently presented standard stimulus. Accordingly, the main habituation effect could also be induced by the repetition of a few uniform tonal stimuli. The degree of habituation was frequency-specific, and comparison across simultaneously recorded units indicated that adaptation effects were apparently topographically organized. At the population level, stronger habituation effects were on average associated with the border regions of the frequency response areas. Finally, the pharmacological inactivation of the auditory cortex demonstrated that SSA in the vMGB is mainly regulated by the corticofugal system. Hence, these results indicate a more general function of SSA in the processing and analysis of auditory information than the term novelty detection suggests.

Gamma rhythms are known to contribute to the process of memory encoding. However, little is known about the underlying mechanisms at the molecular, cellular and network levels. Using local field potential recording in awake behaving mice and concomitant field potential and whole-cell recordings in slice preparations we found that gamma rhythms lead to activity-dependent modification of hippocampal networks, including alterations in sharp wave-ripple complexes. Network plasticity, expressed as long-lasting increases in sharp wave-associated synaptic currents, exhibits enhanced excitatory synaptic strength in pyramidal cells that is induced postsynaptically and depends on metabotropic glutamate receptor-5 activation. In sharp contrast, alteration of inhibitory synaptic strength is independent of postsynaptic activation and less pronounced. Further, we found a cell type-specific, directionally biased synaptic plasticity of two major types of GABAergic cells, parvalbumin- and cholecystokinin-expressing interneurons. Thus, we propose that gamma frequency oscillations represent a network state that introduces long-lasting synaptic plasticity in a cell-specific manner.DOI: http://dx.doi.org/10.7554/eLife.14912.001

The hippocampal output structure, the subiculum, expresses two major memory relevant network rhythms, sharp wave ripple and gamma frequency oscillations. To this date, it remains unclear how the two distinct types of subicular principal cells, intrinsically bursting and regular spiking neurons, participate in these two network rhythms. Using concomitant local field potential and intracellular recordings in an in vitro mouse model that allows the investigation of both network rhythms, we found a cell type-specific segregation of principal neurons into participating intrinsically bursting and non-participating regular spiking cells. However, if regular spiking cells were kept at a more depolarized level, they did participate in a specific manner, suggesting a potential bimodal working model dependent on the level of excitation. Furthermore, intrinsically bursting and regular spiking cells exhibited divergent intrinsic membrane and synaptic properties in the active network. Thus, our results suggest a cell-type-specific segregation of principal cells into two separate groups during network activities, supporting the idea of two parallel streams of information processing within the subiculum.

No abstract