Compartmentalized signaling in the soma: Coordination of electrical and protein kinase A signaling at neuronal ER-plasma membrane junctions.

Neuronal information processing depends on converting membrane depolarizations into compartmentalized biochemical signals that can modify neuronal activity and structure. However, our understanding of how neurons translate electrical signals into specific biochemical responses remains limited, especially in the soma where gene expression and ion channel function are crucial for neuronal activity. Here, I emphasize the importance of physically compartmentalizing action potential-triggered biochemical reactions within the soma. Emerging evidence suggests that somatic endoplasmic reticulum-plasma membrane (ER-PM) junctions are specialized organelles that coordinate electrical and biochemical signaling. The juxtaposition of ion channels and signaling proteins at a prominent subset of these sites enables compartmentalized calcium and cAMP-dependent protein kinase (PKA) signaling. I explore the hypothesis that these PKA-containing ER-PM junctions serve as critical sites for translating membrane depolarizations into PKA signals and identify key gaps in knowledge of the assembly, regulation, and neurobiological functions of this somatic signaling system.

Olfactory receptor neurons are sensitive to stimulus onset asynchrony: implications for odor source discrimination.

In insects, olfactory receptor neurons (ORNs) are localized in sensilla. Within a sensillum, different ORN types are typically co-localized and exhibit nonsynaptic reciprocal inhibition through ephaptic coupling. This inhibition is hypothesized to aid odor source discrimination in environments where odor molecules (odorants) are dispersed by wind, resulting in turbulent plumes. Under these conditions, odorants from a single source arrive at the ORNs synchronously, while those from separate sources arrive asynchronously. Ephaptic inhibition is expected to be weaker for asynchronous arriving odorants from separate sources, thereby enhancing their discrimination. Previous studies have focused on ephaptic inhibition of sustained ORN responses to constant odor stimuli. This begs the question of whether ephaptic inhibition also affects transient ORN responses and if this inhibition is modulated by the temporal arrival patterns of different odorants. To address this, we recorded co-localized ORNs in the fruit fly Drosophila melanogaster and exposed them to dynamic odorant mixtures. We found reciprocal inhibition, strongly suggesting the presence of ephaptic coupling. This reciprocal inhibition does indeed modulate transient ORN responses and is sensitive to the relative timing of odor stimuli. Notably, the strength of inhibition decreases as the synchrony and correlation between arriving odorants decrease. These results support the hypothesis that ephaptic inhibition aids odor source discrimination.

Neuronal Compartmentalization: A Means to Integrate Sensory Input at the Earliest Stage of Information Processing?

In numerous peripheral sense organs, external stimuli are detected by primary sensory neurons compartmentalized within specialized structures composed of cuticular or epithelial tissue. Beyond reflecting developmental constraints, such compartmentalization also provides opportunities for grouped neurons to functionally interact. Here, the authors review and illustrate the prevalence of these structural units, describe characteristics of compartmentalized neurons, and consider possible interactions between these cells. This article discusses instances of neuronal crosstalk, examples of which are observed in the vertebrate tastebuds and multiple types of arthropod chemosensory hairs. Particular attention is paid to insect olfaction, which presents especially well-characterized mechanisms of functional, cross-neuronal interactions. These examples highlight the potential impact of peripheral processing, which likely contributes more to signal integration than previously considered. In surveying a wide variety of structural units, it is hoped that this article will stimulate future research that determines whether grouped neurons in other sensory systems can also communicate to impact information processing.

Synaptic input and temperature influence sensory coding in a mechanoreceptor.

Many neurons possess more than one spike initiation zone (SIZ), which adds to their computational power and functional flexibility. Integrating inputs from different origins is especially relevant for sensory neurons that rely on relative spike timing for encoding sensory information. Yet, it is poorly understood if and how the propagation of spikes generated at one SIZ in response to sensory stimulation is affected by synaptic inputs triggering activity of other SIZ, and by environmental factors like temperature. The mechanosensory Touch (T) cell in the medicinal leech is an ideal model system to study these potential interactions because it allows intracellular recording and stimulation of its soma while simultaneously touching the skin in a body-wall preparation. The T cell reliably elicits spikes in response to somatic depolarization, as well as to tactile skin stimulation. Latencies of spikes elicited in the skin vary across cells, depending on the touch location relative to the cell's receptive field. However, repetitive stimulation reveals that tactilely elicited spikes are more precisely timed than spikes triggered by somatic current injection. When the soma is hyperpolarized to mimic inhibitory synaptic input, first spike latencies of tactilely induced spikes increase. If spikes from both SIZ follow shortly after each other, the arrival time of the second spike at the soma can be delayed. Although the latency of spikes increases by the same factor when the temperature decreases, the effect is considerably stronger for the longer absolute latencies of spikes propagating from the skin to the soma. We therefore conclude that the propagation time of spikes from the skin is modulated by internal factors like synaptic inputs, and by external factors like temperature. Moreover, fewer spikes are detected when spikes from both origins are expected to arrive at the soma in temporal proximity. Hence, the leech T cell might be a key for understanding how the interaction of multiple SIZ impacts temporal and rate coding of sensory information, and how cold-blooded animals can produce adequate behavioral responses to sensory stimuli based on temperature-dependent relative spike timing.