Muscarinic Receptors Control Frequency Tuning Through the Downregulation of an A-Type Potassium Current

The functional role of cholinergic input in the modulation of sensory responses was studied using a combination of in vivo and in vitro electrophysiology supplemented by mathematical modeling. The electrosensory system of weakly electric fish recognizes different environmental stimuli by their unique alteration of a self-generated electric field. Variations in the patterns of stimuli are primarily distinguished based on their frequency. Pyramidal neurons in the electrosensory lateral line lobe (ELL) are often tuned to respond to specific input frequencies. Alterations in the tuning of the pyramidal neurons may allow weakly electric fish to preferentially select for certain stimuli. Here we show that muscarinic receptor activation in vivo enhances the excitability, burst firing, and subsequently the response of pyramidal cells to naturalistic sensory input. Through a combination of in vitro electrophysiology and mathematical modeling, we reveal that this enhanced excitability and bursting likely results from the down-regulation of an A-type potassium current. Further, we provide an explanation of the mechanism by which these currents can mediate frequency tuning.

Download Full-text

Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe

Journal of Experimental Biology ◽

10.1242/jeb.202.10.1255 ◽

1999 ◽

Vol 202 (10) ◽

pp. 1255-1265 ◽

Cited By ~ 1

Author(s):

R.W. Turner ◽

L. Maler

Keyword(s):

Feature Extraction ◽

Lateral Line ◽

Pyramidal Cell ◽

Frequency Tuning ◽

Pyramidal Cells ◽

Weakly Electric Fish ◽

Burst Discharge ◽

Sensory Maps

Oscillatory and burst discharge is recognized as a key element of signal processing from the level of receptor to cortical output cells in most sensory systems. The relevance of this activity for electrosensory processing has become increasingly apparent for cells in the electrosensory lateral line lobe (ELL) of gymnotiform weakly electric fish. Burst discharge by ELL pyramidal cells can be recorded in vivo and has been directly associated with feature extraction of electrosensory input. In vivo recordings have also shown that pyramidal cells are differentially tuned to the frequency of amplitude modulations across three ELL topographic maps of electroreceptor distribution. Pyramidal cell recordings in vitro reveal two forms of oscillatory discharge with properties consistent with pyramidal cell frequency tuning in vivo. One is a slow oscillation of spike discharge arising from local circuit interactions that exhibits marked changes in several properties across the sensory maps. The second is a fast, intrinsic form of burst discharge that incorporates a newly recognized interaction between somatic and dendritic membranes. These findings suggest that a differential regulation of oscillatory discharge properties across sensory maps may underlie frequency tuning in the ELL and influence feature extraction in vivo.

Download Full-text

Tectal input to the central posterior/prepacemaker nucleus of weakly electric fish, Apteronotus leptorhynchus : an in vitro tract-tracing study

Brain Research ◽

10.1016/s0006-8993(96)00818-9 ◽

1996 ◽

Vol 739 (1-2) ◽

pp. 201-209 ◽

Cited By ~ 13

Author(s):

Günther K.H. Zupanc ◽

Ingrid Horschke

Keyword(s):

Electric Fish ◽

Weakly Electric Fish ◽

Apteronotus Leptorhynchus ◽

Tract Tracing ◽

Weakly Electric

Download Full-text

An in vitro physiological preparation of a vertebrate communicatory behavior: chirping in the weakly electric fish,Apteronotus

Journal of Comparative Physiology A ◽

10.1007/bf00604899 ◽

1988 ◽

Vol 163 (4) ◽

pp. 445-458 ◽

Cited By ~ 26

Author(s):

John Dye

Keyword(s):

Electric Fish ◽

Weakly Electric Fish ◽

Weakly Electric

Download Full-text

Sensory tuning does not match behavioral relevance of communication signals in free-living weakly electric fish

10.1101/114249 ◽

2017 ◽

Cited By ~ 3

Author(s):

Jörg Henninger ◽

Rüdiger Krahe ◽

Frank Kirschbaum ◽

Jan Grewe ◽

Jan Benda

Keyword(s):

Electric Fish ◽

Frequency Tuning ◽

Neuronal Population ◽

Weakly Electric Fish ◽

Ecological Niches ◽

Natural Habitats ◽

Population Activity ◽

Communication Signals ◽

Spatio Temporal ◽

Weakly Electric

AbstractSensory systems evolve in the ecological niches each species is occupying. Accordingly, the tuning of sensory neurons is expected to be adapted to the statistics of natural stimuli. For an unbiased quantification of sensory scenes we tracked natural communication behavior of the weakly electric fish Apteronotus rostratus in their Neotropical rainforest habitat with high spatio-temporal resolution over several days. In the context of courtship and aggression we observed large quantities of electrocommunication signals. Echo responses and acknowledgment signals clearly demonstrated the behavioral relevance of these signals. The known tuning properties of peripheral electrosensory neurons suggest, however, that they are barely activated by these obviously relevant signals. Frequencies of courtship signals are clearly mismatched with the frequency tuning of neuronal population activity. Our results emphasize the importance of quantifying sensory scenes derived from freely behaving animals in their natural habitats for understanding the evolution and function of neural systems.

Download Full-text

Fiber connections of the diencephalic nucleus tuberis anterior in the weakly electric fish,Gymnotus cf. carapo: An in vivo tract-tracing study

The Journal of Comparative Neurology ◽

10.1002/cne.21413 ◽

2007 ◽

Vol 503 (5) ◽

pp. 655-667 ◽

Cited By ~ 6

Author(s):

Ana Catarina Casari Giassi ◽

Sonia Aparecida Lopes Corrêa ◽

Anette Hoffmann

Keyword(s):

Electric Fish ◽

Weakly Electric Fish ◽

Tract Tracing ◽

Weakly Electric

Download Full-text

Detection of transient synchrony across oscillating receptors by the central electrosensory system of mormyrid fish

eLife ◽

10.7554/elife.16851 ◽

2016 ◽

Vol 5 ◽

Cited By ~ 9

Author(s):

Alejandro Vélez ◽

Bruce A Carlson

Keyword(s):

Electric Fish ◽

Frequency Tuning ◽

Weakly Electric Fish ◽

Sensory Coding ◽

Electrosensory System ◽

Mormyrid Fish ◽

Intrinsic Oscillation ◽

Oscillation Frequencies ◽

Weakly Electric ◽

Peripheral Sensory

Recently, we reported evidence for a novel mechanism of peripheral sensory coding based on oscillatory synchrony. Spontaneously oscillating electroreceptors in weakly electric fish (Mormyridae) respond to electrosensory stimuli with a phase reset that results in transient synchrony across the receptor population (<xref ref-type="bibr" rid="bib5">Baker et al., 2015</xref>). Here, we asked whether the central electrosensory system actually detects the occurrence of synchronous oscillations among receptors. We found that electrosensory stimulation elicited evoked potentials in the midbrain exterolateral nucleus at a short latency following receptor synchronization. Frequency tuning in the midbrain resembled peripheral frequency tuning, which matches the intrinsic oscillation frequencies of the receptors. These frequencies are lower than those in individual conspecific signals, and instead match those found in collective signals produced by groups of conspecifics. Our results provide further support for a novel mechanism for sensory coding based on the detection of oscillatory synchrony among peripheral receptors.

Download Full-text