The Origin of Adaptation in the Auditory Pathway of Locusts Is Specific to Cell Type and Function

Abstract

We investigated the origin of spike frequency adaptation within a layered sensory network: the auditory pathway of locusts. Spike frequency adaptation as observed in an individual neuron may arise because of intrinsic or presynaptic adaptation mechanisms. To separate the contribution of different mechanisms, we recorded from the same cell during acoustic and intracellular current stimulation. We studied three identified neuron types that are representative for each network layer and participate in processing auditory patterns and localizing sound sources. By comparing current and acoustic stimulation, three distinct patterns of the distribution of adaptation mechanisms within the sensory network emerged: (1) balanced influence of both intrinsic and presynaptic adaptation mechanisms in an interneuron that summates over several receptor afferents (TN1), (2) predominantly inhibiting input as the source for spike frequency adaptation in a cell that transmits both pattern representation and directional information (BSN1), (3) primarily intrinsic, spiketriggered adaptation currents within an interneuron coding exclusively for direction (AN2). The time courses of spike frequency adaptation differed significantly between the cells types. Using the adaptation time constants, we were able to predict signal transmission properties for the different cells. We conclude that the adaptation mechanisms differ greatly among interneurons within this sensory pathway and are a function of their role in information processing.

Multiple Arithmetic Operations in a Single Neuron: The Recruitment of Adaptation Processes in the Cricket Auditory Pathway Depends on Sensory Context

“…4C). It is likely that the subtractive effect is a combination of the adaptation currents in AN2 and adaptation mechanisms located more peripherally, either in the receptor neurons or at the synapses, a pattern that has also been reported in the auditory system of grasshoppers (Hildebrandt et al, 2009).…”

“…This is most relevant for test stimuli smaller than the background (duration 100 ms), and in these cases, we would have underestimated spike frequencies Ͻ20 Hz. However, almost all of the suprathreshold response curve of the AN2 were far above 20 Hz as can be seen for the unadapted curves, which were measured using 500 ms test stimuli (for more details, see Hildebrandt et al, 2009). …”

Efficient transformation of an auditory population code in a small sensory system

“…Hence, the labeled-line code observed at the third neuronal layer is not explicitly derived from another labeled-line code, but has to be established de novo by a transformation of the stimulus representation in the first two layers. The construction of this labeled line from uniformly tuned inputs is presumably achieved by adaptation and a well-timed interplay of excitation and inhibition (30,31).…”

Nonlinear Computations Underlying Temporal and Population Sparseness in the Auditory System of the Grasshopper

“…4h), which are possibly implemented in a network: the STA filter corresponds to excitatory inputs and drives the cell; as the STC filter leads the STA and is suppressive, the cell will only fire strongly if the stimulus preceding the STA is relatively soft. Such an implementation is highly likely for the phasic BSN1, AN1, and AN3, for which strong, slow inhibitory inputs have been shown in dendritic recordings (Römer and Marquart, 1984;Hildebrandt et al, 2009). For another leading-suppressive cell type in our dataset-AN2-a strong afterhyperpolarization has been shown to underlie adaptation (Hildebrandt et al, 2009); yet, this cell also receives contralateral inhibition that can be slower than the excitation.…”

“…Such an implementation is highly likely for the phasic BSN1, AN1, and AN3, for which strong, slow inhibitory inputs have been shown in dendritic recordings (Römer and Marquart, 1984;Hildebrandt et al, 2009). For another leading-suppressive cell type in our dataset-AN2-a strong afterhyperpolarization has been shown to underlie adaptation (Hildebrandt et al, 2009); yet, this cell also receives contralateral inhibition that can be slower than the excitation. The STC filter of this cell type is thus likely to be a combination of both cell-intrinsic adaptive currents and inhibitory inputs.…”