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The Journal of Neuroscience, August 20, 2003, 23(20):7489-7503

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Connexin35 Mediates Electrical Transmission at Mixed Synapses on Mauthner Cells

A. Pereda,¹ J. O'Brien,² J. I. Nagy,³ F. Bukauskas,¹ K. G. V. Davidson,⁴ N. Kamasawa,⁴ T. Yasumura,⁴ and J. E. Rash⁴

¹Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461, ²Department of Ophthalmology and Visual Science, University of Texas at Houston-Health Science Center, Houston, Texas 77030, ³Department of Physiology, University of Manitoba, Winnipeg R3E 3J7, Canada, and ⁴Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado 80523

Auditory afferents terminating as "large myelinated club endings" on goldfish Mauthner cells are identifiable "mixed" (electrical and chemical) synaptic terminals that offer the unique opportunity to correlate physiological properties with biochemical composition and specific ultrastructural features of individual synapses. By combining confocal microscopy and freeze-fracture replica immunogold labeling (FRIL), we demonstrate that gap junctions at these synapses contain connexin35 (Cx35). This connexin is the fish ortholog of the neuron-specific human and mouse connexin36 that is reported to be widely distributed in mammalian brain and to be responsible for electrical coupling between many types of neurons. Similarly, connexin35 was found at gap junctions between neurons in other brain regions, suggesting that connexin35-mediated electrical transmission is common in goldfish brain. Conductance of gap junction channels at large myelinated club endings is known to be dynamically modulated by the activity of their colocalized glutamatergic synapses. We show evidence by confocal microscopy for the presence of the NR1 subunit of the NMDA glutamate receptor subtype, proposed to be a key regulatory element, at these large endings. Furthermore, we also show evidence by FRIL double-immunogold labeling that the NR1 subunit of the NMDA glutamate receptor is present at postsynaptic densities closely associated with gap junction plaques containing Cx35 at mixed synapses across the goldfish hindbrain. Given the widespread distribution of electrical synapses and glutamate receptors, our results suggest that the plastic properties observed at these identifiable junctions may apply to other electrical synapses, including those in mammalian brain.

Key words: gap junction; connexin36; electrical synapse; NMDA; synaptic plasticity; electrical coupling; auditory

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Received Sep 10, 2002; revised June 19, 2003; accepted June 24, 2003.

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