GABAergic inhibition shapes temporal and spatial response properties of pyramidal cells in the electrosensory lateral line lobe of gymnotiform fish

Abstract

1. The amplitude-coding pyramidal neurons of the first-order nucleus in weakly electric gymnotiform fish (Eigenmannia), the electrosensory lateral line lobe (ELL), exhibit 2 major physiological transformations of primary afferent input. Pyramidal cells rapidly adapt to a step change in amplitude, and they have a center/surround receptive-field organization. This study examined the physiological role of GABAergic inhibition on pyramidal cells. GABAergic synapses onto the somata of pyramidal cells primarily originate from granule-cell interneurons along with descending input. 2. Pyramidal cells fall into two physiologically distinct categories: E units, which are excited by a rise in stimulus amplitude, and I units, which are inhibited by a rise in stimulus amplitude. Microiontophoretic application of bicuculline methiodide onto both types of pyramidal cells increased the time constant of adaptation, defined as the time required for the neuron's response to decay to 37% of its maximum value, by 70-90%. The peak firing rate of E units to a step increase in stimulus amplitude increased by 49%, while the firing rate of I units did not change significantly. 3. Bicuculline application demonstrated that GABAergic inhibition may contribute to the strict segregation of E and I response properties. In the presence of bicuculline, many E units (normally excited only by stimulus amplitude increases) became excited by both increases and decreases; many I units (normally excited only by amplitude decreases) also became excited to increases. 4. The size of the excitatory receptive-field of E units was not affected by bicuculline, although response magnitude increased. The inhibitory surround increased in spatial extent by 175% with bicuculline administration. Neither the size of the I unit receptive-field center nor the response magnitude changed in the presence of bicuculline. The antagonistic surround of I units, however, increased by 49%. 5. The anatomy of the ELL is well understood (see Carr and Maler 1986). The physiological results obtained in this study, along with the results of Bastian (1986a, b), further our understanding of the functional role of the ELL circuitry. Our results suggest that spatial and temporal response properties of pyramidal cells are regulated by different but interacting inhibitory interneurons, some of which use GABA as a neurotransmitter. The activity of these interneurons is in turn controlled by descending feedback systems.

Descending control of electroreception. I. Properties of nucleus praeeminentialis neurons projecting indirectly to the electrosensory lateral line lobe

“…This compensation is expected to occur in the central nervous system (CNS) since no efferents are known to project to the electroreceptors. This control seems to be primarily mediated via inhibitory mechanisms since local microinjection of GABA antagonists causes changes in ELL physiology similar to those due to lesions of the descending input to the EGP (Shumway and Maler, 1989). In this and in the following report (Bratton and Bastian, 1990) we describe the functional characteristics of NPd neurons that project to the ELLS via the indirect and direct pathways.…”

“…These EOD distortions cause changes in the firing frequency and timing of electroreceptor afferents which terminate somatotopically within the electrosensory lateral line lobe (ELL) (Carr et al, 1982;Heiligenberg and Dye, 1982). The ELL, a complex laminated structure, has been intensively studied anatomically (Rethelyi and Szabo, 1973;Maler et al, 1974Maler et al, , 1981Maler, 1979;Shumway, 1989b) and physiologically Bastian, 198 1 b;Saunders and Bastian, 1984;Mathieson and Maler, 1988;Shumway, 1989a;Shumway and Maler, 1989). The output of the ELL projects primarily contralaterally to the midbrain, terminating in the torus semicircularis and in an isthmic structure, the nucleus praeeminentialis pars dorsalis (NPd).…”

Frequency-Tuned Cerebellar Channels and Burst-Induced LTD Lead to the Cancellation of Redundant Sensory Inputs

“…4B). This minor discrepancy may be due to intrinsic (Mehaffey et al, 2005) or feedforward inhibitory (Shumway and Maler, 1989) adaptation dynamics that were not included in our model. Nonlinear synaptic depression from very large bursts not included in the model may also be a factor.…”

Similar Algorithms in Different Sensory Systems and Animals

“…3 and 4) (Sullivan and Konishi 1986;Carr and Konishi 1988). In the electric fish, circuits for the comparison of the phase angle and amplitude of electrical signals between different body areas have been identified (Maler 1979;Carr et al 1986a,b;Shumway and Maler 1989). …”