Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

Abstract

Acute temperature changes can disrupt neuronal activity and coordination with severe consequences for animal behavior and survival. Nonetheless, two rhythmic neuronal circuits in the crustacean stomatogastric ganglion (STG) and their coordination are maintained across a broad temperature range. However, it remains unclear how this temperature robustness is achieved. Here, we dissociate temperature effects on the rhythm generating circuits from those on upstream ganglia. We demonstrate that heat-activated factors extrinsic to the rhythm generators are essential to the slow gastric mill rhythm’s temperature robustness and contribute to the temperature response of the fast pyloric rhythm. The gastric mill rhythm crashed when its rhythm generator in the STG was heated. It was restored when upstream ganglia were heated and temperature-matched to the STG. This also increased the activity of the peptidergic modulatory projection neuron (MCN1), which innervates the gastric mill circuit. Correspondingly, MCN1’s neuropeptide transmitter stabilized the rhythm and maintained it over a broad temperature range. Extrinsic neuromodulation is thus essential for the oscillatory circuits in the STG and enables neural circuits to maintain function in temperature-compromised conditions. In contrast, integer coupling between pyloric and gastric mill rhythms was independent of whether extrinsic inputs and STG pattern generators were temperature-matched or not, demonstrating that the temperature robustness of the coupling is enabled by properties intrinsic to the rhythm generators. However, at near-crash temperature, integer coupling was maintained only in some animals while it was absent in others. This was true despite regular rhythmic activity in all animals, supporting that degenerate circuit properties result in idiosyncratic responses to environmental challenges.

A review of the bioeffects of low-intensity focused ultrasound and the benefits of a cellular approach

“…Given the leech's ability to maintain neural firing across significant environmental temperature changes, owing presumably to similar compensation mechanisms to those described in other organisms (Robertson and Money, 2012;Städele et al, 2015;Städele and Stein, 2022), we were initially surprised that artificial temperature increases as low as 2 °C could cause the dramatic modulation of neural activity we observed (Collins et al, 2021). One key difference between our heating modalities and those employed in most studies examining temperature compensation is the spatial gradient of the temperature increase.…”

The role of feedback and modulation in determining temperature resiliency in the lobster cardiac nervous system

“…A number of studies have found that signaling molecules and feedback modulation play a role in maintaining circuit function even though the molecular kinetics of all cellular components are altered due to changes in temperature ( Zhurov and Brezina, 2005 ; Hamilton et al, 2007 ; Biron et al, 2008 ; Tang et al, 2010 ; Thuma et al, 2013 ; Städele et al, 2015 ; Haddad and Marder, 2018 ; Takeishi et al, 2020 ; Städele and Stein, 2022 ). As such, we were particularly interested in examining the role of feedback in determining the crash temperature in this neuromuscular system.…”

“…Because each ion channel type can be differently affected by changes in temperature, predicting how temperature change will affect even a single neuron is not simple (Caplan et al, 2014;O'Leary and Marder, 2016;Alonso and Marder, 2020). These predictions are even more difficult to understand when extrapolating to neural circuits, as synaptic (Tang et al, 2010;Rinberg et al, 2013;Soofi et al, 2014;Städele et al, 2015;O'Leary and Marder, 2016;Alonso and Marder, 2020;Powell et al, 2021;Ratliff et al, 2021;Städele and Stein, 2022) and muscle physiology (Harri and Florey, 1977;Foldes et al, 1978;Rutkove, 2001;Racinais and Oksa, 2010;Thuma et al, 2013;Kushinsky et al, 2019; this paper) are also affected. Some processes of temperature compensation in the neural circuits of poikilotherms have been revealed (Harri and Florey, 1977;Foldes et al, 1978;Rutkove, 2001;Racinais and Oksa, 2010;Kushinsky et al, 2019).…”

“…For example, within the stomatogastric ganglion (STG) of the Jonah crab, there are two coupled pattern generating circuits. While each circuit has different processes that enable temperature compensation, they are both able to maintain function across a similar range of temperature (∼7–30°C) ( Tang et al, 2010 ; Tang et al, 2012 ; Rinberg et al, 2013 ; Soofi et al, 2014 ; Städele et al, 2015 ; Haddad and Marder, 2018 ; Powell et al, 2021 ; Ratliff et al, 2021 ; Städele and Stein, 2022 ). For instance, one such compensatory process includes similar increases in maximal conductance and gating rates for Na + and K + mediated ion channel currents that contribute to bursting (I h , I A , and synaptic currents).…”

“…Here we investigate how both feedback and feedforward processes contribute to temperature resiliency in the cardiac neuromuscular system. Many studies have focused on how modulatory input increases the temperature tolerance of nervous systems ( Städele et al, 2015 ; Haddad and Marder, 2018 ; DeMaegd and Stein, 2021 ; Städele and Stein, 2022 ). There are also a few that indicate either directly ( Srithiphaphirom et al, 2019 ) or indirectly ( Alonso and Marder, 2020 ) that decreasing neural excitability decreases temperature tolerance.…”