Parallel Projection of Amplitude and Phase Information from the Hindbrain to the Midbrain of the African Electric FishGymnarchus niloticus

Abstract

Two distinct sensory cues in electrosensory signals, amplitude modulation and differential phase modulation, are essential for an African wave-type electric fish, Gymnarchus, to perform the jamming avoidance responses. Individual neurons in the first brain station for central processing, the electrosensory lateral line lobe (ELL), were investigated by the in vivo whole-cell recording and labeling technique for their physiological responses, location, morphology, and projection areas. Neurons in the dorsal zone of the ELL responded selectively to amplitude modulation. Neurons in the outer cell layer of the medial zone were categorized physiologically into two groups: amplitude-sensitive and differential phase-sensitive. All but one neuron in the inner cell layer of the medial zone responded exclusively to differential phase modulation. All neurons recorded and labeled in the ELL had pyramidal morphology with large and extensive apical dendrites and less extensive basal dendrites. They were found to project to two midbrain nuclei: the nucleus praeeminentialis and the torus semicircularis. Amplitude-sensitive neurons in the dorsal zone projected exclusively to the lateral posterior subdivision, the torus semicircularis. Neurons in the medial zone projected to the medial dorsal and lateral anterior subdivisions of the torus semicircularis. Although some neurons in the ELL responded to both amplitude and differential phase modulation, they did not differentiate between temporal patterns of the two cues that encode necessary information for the jamming avoidance response. Overlapping projection of amplitude and differential phase-sensitive neurons to the torus semicircularis suggests integration of the two sensory cues in this nucleus.

Multiple Cases of Striking Genetic Similarity Between Alternate Electric Fish Signal Morphs in Sympatry

“…These ELL neurons respond identically to either sense of rotation, because they respond only to a parameter belonging to one axis of the graph, the amplitude or time difference, each of which follows an identical time course for either sense of rotation. These neurons do not interact with each other in the ELL, but project to common areas in the midbrain (Kawasaki and Guo, 1998). There, 'sign selective' neurons selectively respond to the sense of rotation of these two stimulus parameters (Carlson and Kawasaki, 2004;Kawasaki and Guo, 2002).…”

From stimulus estimation to combination sensitivity: encoding and processing of amplitude and timing information in parallel, convergent sensory pathways

“…For recordings from hindbrain ELL pyramidal neurons, we removed a small portion of the skull and meninges above the corpus cerebelli (Kawasaki andGuo 1996Kawasaki andGuo 1998), and exposed the dorsal surface of the ELL by using the grounding wire to displace the corpus cerebelli. For recordings from torus semicircularis neurons, we removed a small portion of the skull and meninges above the midbrain, and exposed the dorsal surface of the torus semicircularis by using the grounding wire to displace the valvula cerebelli.…”

“…The amplitude-coding pathway of Gymnarchus exhibits a similar organization to gymnotiforms, with O-afferents projecting to AM-sensitive pyramidal neurons in the hindbrain ELL (Kawasaki and Guo 1998). Unlike gymnotiforms, in which PM information is extracted in the midbrain (Carr et al 1986a;Carr et al 1986b), S-afferents in Gymnarchus give rise to PM-sensitive pyramidal neurons in the ELL through a combination of direct and indirect synaptic inputs (Kawasaki andGuo 1996Kawasaki andGuo 1998;Matsushita and Kawasaki 2004).…”

“…Unlike gymnotiforms, in which PM information is extracted in the midbrain (Carr et al 1986a;Carr et al 1986b), S-afferents in Gymnarchus give rise to PM-sensitive pyramidal neurons in the ELL through a combination of direct and indirect synaptic inputs (Kawasaki andGuo 1996Kawasaki andGuo 1998;Matsushita and Kawasaki 2004). Both AM-and PM-sensitive pyramidal neurons project to the midbrain torus semicircularis, where the amplitude-and time-coding pathways converge (Kawasaki and Guo 1998), and many neurons are sensitive to particular combinations of AM and PM (Kawasaki and Guo 2002;Kawasaki 2004, 2006b), similar to the convergence of amplitudeand time-coding pathways in the midbrain of the barn owl auditory system (Knudsen and Konishi 1978;Peña and Konishi 2001). …”

Energy, information, detection, and action

“…Indeed, this parallel organization is essential for optimum processing efficiency, as different neurons and pathways are specialized for processing certain aspects of a stimulus. Examples of this are the channels coding form and motion in the mammalian visual pathway (Livingstone & Hubel 1988), the time and intensity channels of the auditory pathway (Feldman & Knudsen 1997), or the amplitude and phase channels in the electrosensory pathway (Kawasaki & Guo 1998). In these cases, the neurons and synapses in each pathway are designed optimally for the task at hand.…”