Electrophysiological Properties of Octopus Neurons of the Cat Cochlear Nucleus: an In Vitro Study

Abstract

Electrophysiological studies from mice in vitro have suggested that octopus cells of the mammalian ventral cochlear nucleus (VCN) are anatomically and biophysically specialized for detecting the coincident firing of a population of auditory nerve fibers. Recordings from cats in vivo have shown that octopus cells fire rapidly and with exceptional temporal precision as they convey the timing of that coincidence to higher auditory centers. The current study addresses the question whether the biophysical properties of octopus cells that have until now been examined only in mice, are shared by octopus cells in cats. Whole-cell patch-clamp recordings confirm that octopus cells in brain slices from kittens share the anatomical and biophysical features of octopus cells in mice. As in mice, octopus cells in kittens have large cell bodies and thick dendrites that extend in one direction. Voltage changes produced by depolarizing and hyperpolarizing current injection were small and rapid. Input resistances and membrane time constants in octopus cells of 16-day-old kittens were 15.8± 1.5 MΩ (n=16) and 1.28±0.3 ms (n=16), respectively. Octopus cells fired only a single action potential at the onset of a depolarizing current pulse; suprathreshold stimuli were greater than 1.8 nA. A tetrodotoxin (TTX)-sensitive sodium conductance (g Na ) was responsible for the generation of the action potentials. Octopus cells displayed outward rectification that lasted for the duration of the depolarizing pulses. Hyperpolarizations produced by the injection of current exhibited a depolarizing sag of the membrane potential toward the resting value. A 4-aminopyridine (4-AP) and α-dendrotoxin (α-DTX)-sensitive, lowvoltage-activated potassium conductance (g KL ) and a ZD7288-sensitive, mixed-cation conductance (g h ) were partially activated at rest, giving the octopus cells low input resistances and, as a consequence, brief time constants. In 7-day-old kittens, action potentials were taller and broader, input resistances higher, and both inward and outward rectification was weaker than in 16-day-old kittens. Also as in mice, stellate cells of the VCN fired trains of action potentials with constant interspike intervals when they were depolarized (n=10) and bushy cells of the VCN fired only a single action potential at the onset of depolarizations (n=6). In conclusion, the similarity of octopus cells in mice and kittens suggests that the anatomical and biophysical specializations that allow octopus cells to detect and convey synchronous firing among auditory nerve fibers are common to all mammals.

Electrophysiological properties of ventral cochlear nucleus neurons of the dog

“…The dendritic and somatic morphologies of the biocytin-labeled stellate, bushy and octopus cells were consistent with previous reports (Osen, 1969;Brawer et al, 1974;Kane, 1973;Webster and Trune, 1982;Rhode et al, 1983;Oertel et al, 1990;Golding et al, 1995Golding et al, , 1999Cao et al, 2007;Bal and Baydas, 2009). …”

“…The onset responsiveness to depolarizing pulses, the rectification in the depolarizing voltage range and depolarizing sags of the membrane potential towards the resting value in responses to hyperpolarizing current pulses were striking properties of the bushy cells in the current study and are consistent with bushy cells in the mouse and cat (Oertel et al, 1990;Manis and Marx, 1991;Cao et al, 2007;Bal and Baydas, 2009). The amplitude of the action potentials in the bushy cells was surprisingly large (73 mV) in dog compared to that in mice, but similar to that of kittens.…”

“…The bushy cells of the dog VCN in the current study have a pattern of biophysical specializations consistent with those of mice and cats (see Table 1) (Oertel et al, 1990;Manis and Marx, 1991;Cao et al, 2007;Bal and Baydas, 2009). The onset responsiveness to depolarizing pulses, the rectification in the depolarizing voltage range and depolarizing sags of the membrane potential towards the resting value in responses to hyperpolarizing current pulses were striking properties of the bushy cells in the current study and are consistent with bushy cells in the mouse and cat (Oertel et al, 1990;Manis and Marx, 1991;Cao et al, 2007;Bal and Baydas, 2009).…”

“…Octopus cells were initially identified in the second and third 160 lmthick coronal CN slices from the caudal side by their large size and characteristic location in the octopus cell area, a region in which there is no apparent intermingling with the other cells, and then by their response pattern. Outside the octopus cell area in the VCN where stellate and bushy cells were intermingled, the identification of bushy and stellate cells were electrophysiologically unambiguous in dogs, as in mice and cats (Oertel, 1983;Fujino and Oertel, 2001;Rodrigues and Oertel, 2006;Cao et al, 2007;Bal and Baydas, 2009). The octopus cells and bushy cells responded with a single action potential at current onset, independent of the strength of the current, but the stellate cells fired trains of action potentials with constant interspike intervals when they were depolarized by the injection of current pulses.…”

“…The biophysical properties of stellate, bushy and octopus cells have successfully been characterized in mice, rat, gerbil, guinea pig and cats (Oertel, 1983;Golding et al, 1995Golding et al, , 1999Fujino and Oertel, 2001;Rodrigues and Oertel, 2006;Schwarz and Puil, 1997;Isaacson and Walmsley, 1996;Rusznák et al, 1996;Cao et al, 2007;Bal and Oertel, 2000Bal and Baydas, 2009). In vitro recordings have shown that octopus and bushy cells fire only one action potential at the onset of a suprathreshold depolarizing current pulse, whereas stellate cells fire tonically in response to the same stimulus Oertel, 1983;Schwarz and Puil, 1997).…”