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Neurobiology, Behavior, and Evolution of Electrosensory Processing in Eigenmannia


Carver, S., Roth, E., Cowan, N.J. and E.S. Fortune, (2008) Synaptic Plasticity Can Produce and Enhance Direction Selectivity. PLoS Comput. Biol., 4(2): e32. doi:10.1371/journal.pcbi.0040032.

A model that demonstrates how two time constants associated with short-term synaptic depression - a fast time constant on the order of milliseconds to seconds and a slower time constant on the order of seconds to tens of seconds - contribute to the generation and enhancement of direction selectivity. The model captures the major features observed in a population of direction-selective midbrain neurons in the electrosensory midbrain of Eigenmannia virescens.
Cowan, N.J. and E.S. Fortune, (2007) The critical role of locomotion mechanics in decoding sensory systems. J. Neurosci, 27:1123-1128.

Simple measurements - the position of the fish - were made during an image-stabilization task where fish swim back and forth to maintain position within a moving refuge. Using basic laws of swimming mechanics, we made a model for sensory computations necessary for the control of the motor system during the task. The model matched neurophysiological properties of the electrosensory system in these fish. These physiological properties, particularly high-pass filtering of sensory signals, are found in a wide array of sensory systems and may reflect a common role for in motor control.
Fortune, E.S. (2006) The decoding of electrosensory systems. Curr. Opin. Neurobiol., doi:10.1016/j.conb.2006.06.006.

This review was written to be accessible for a broad neuroscience audience. Towards this end, examples from the visual system are used to illustrate the features of certain electrosensory stimuli.
Ramcharitar, J.U., Tan, E.W., E.S. Fortune (2006) Global electrosensory oscillations enhance directional responses of midbrain neurons in Eigenmannia. J. Neurophys., doi:10.1152/jn.00311.2006.

Characterizes the responses of midbrain neurons to moving objects in the presence and absence of post-Jamming-Avoidance-Response global stimuli.
Fortune, E.S., Rose, G.J., and M. Kawasaki (2006) Encoding and processing biologically relevant temporal information in electrosensory systems. J. Comp. Physiol. A, 192:625-635.

A broad review of electrosensory encoding of temporal information (from microseconds to seconds) for the control of jamming avoidance response behaviors.
Tan, E.W., Nizar, J.M., Carrera-G, E., and E.S. Fortune (2005) Electrosensory interference in naturally occurring aggregates of a species of weakly electric fish, Eigenmannia virescens. Behav. Brain Res., 164:83-92.

Characterizes the electric fields that are most commonly experienced by Eigenmannia both in the upper Amazon of Ecuador and in laboratory settings. Eigenmannia are preferentially found in groups and experience ongoing high-frequency (> 20 Hz) global oscillations.
Ramcharitar, J.U., Tan, E.W., and E.S. Fortune (2005) Effects of global electrosensory signals on motion processing in the midbrain of Eigenmannia. J. Comp. Physiol. A, 191:865-872.

Characterizes the magnitudes of the responses of midbrain neurons to moving objects in the presence and absence of global electrosensory stimuli.
Fortune, E.S. and G.J. Rose (2003) Voltage-gated Na+ channels enhance the temporal filtering properties of electrosensory neurons in the torus. J. Neurophys., 90:924-929.

Demonstrates the existance of two types of all-or-none PSPs in toral electrosensory neurons in Eigenmannia virescens. The first type, constant duration or "CD" PSPs can be 1) elicited by current injection alone and 2) are eliminated by application of sodium-channel blockers QX-222 and QX-314. CD PSPs appear to enhance responses to social communication signals. The second type, variable duration or "VD" PSPs are not elicited by current injection alone and are not blocked by QX drugs. These PSPs apparently require both synaptic input and depolarization for activation. VD PSPs enhance responses to signals that can elicit the jamming avoidance response, and may be mediated by NMDARs.
Fortune, E.S. and G.J. Rose (2002) Roles for short-term synaptic plasticity in behavior. J Physiol Paris, 96:539-545.

A review of data obtained in midbrain electrosensory neurons of Eigenmannia that suggest plasticity has at least two roles in sensory processing; enhancing low-pass temporal filtering and generating phase shifts used in processing moving sensory images.
Fortune, E.S. and G.J. Rose (2001) Short-term synaptic plasticity as a temporal filter. Trends in Neurosciences, 24:381-385.

This Opinion article argues that synaptic plasticity in sensory systems of many vertebrate species, including mammals, should be considered a mechanism for dynamic temporal filtering. A sub-theme is that natural patterns of afferent activity are necessary to assess the functional roles of the interplay between synaptic depression and facilitation.
Fortune, E.S., and G.J. Rose (2000) Short-term synaptic plasticity contributes to the temporal filtering of electrosensory information, J. Neurosci., 20:7122-7130.
Intracellular recordings from midbrain neurons in awake, behaving animals demonstrate the dynamics and functional roles of short-term synaptic plasticity. Short-term depression enhances low-pass temporal filtering and allows responses to sensory transients, and short-term facilitation maintains responses to low-frequency information in the presence of depressing, high frequency information.
Rose, G.J. and E.S. Fortune (1999) Frequency-dependent PSP depression contributes to low-pass temporal filtering in Eigenmannia. J. Neurosci., 19:7629-7639.
Behavioral and neuropysiological data demonstrate that short-term depression can act to enhance low-pass temporal filtering.
Rose, G.J. and E.S. Fortune (1999) Mechanisms for generating temporal filters in the electrosensory system. J. Exp. Biol., 202:1281-1289.
A review article summarizing the constellation of mechanisms that midbrain neurons employ to generate low-, band- , and high-pass temporal filtering properties.
Fortune, E.S. and G.J. Rose (1997) Passive and active membrane properties contribute to the temporal filtering properties of midbrain neurons, in vivo. J. Neurosci., 17:3815-3825.
Biophysical measurements of membrane properties were made in vivo to assess and quantify how passive and active electrical characteristics of neurons affect their functional properties. Because all neurons in all animals have such electrical properties, these data are widely applicable.
Fortune, E.S. and G.J. Rose (1997) Temporal filtering properties of ampullary electrosensory neurons in the torus semicircularis of Eigenmannia: evolutionary and computational implications. Brain, Behav., and Evol., 49:312-323.
A comparison of the properties of the phylogenetically ancient ampullary system with the evolutionarily novel tuberous (p-type) system. The two systems share many anatomical and physiological features, which is consistent with the hypothesis that the tuberous system is a elaboration or duplication of the ampullary system.
Rose, G.J. and E.S. Fortune (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci. Res. 26:89-94.
A technical note describing details of how to make intracellular recordings from neurons in vivo using low-resistance patch-type pipettes.


Structure, Function, and Evolution of Brain Structures for Singing in Oscine Birds


Fortune, E.S. and D. Margoliash (1995) Parallel pathways and convergence onto HVc and adjacent neostriatum of adult male zebra finches (Taeniopygia guttata). J. Comp. Neurol. 360(3): 413-441.
This paper has two major parts: a critical definition of HVc based on Nissl stained material and the connectivity of HVc and adjacent areas based in injection of tracers. There are three major conclusions: 1. HVc is composed of 3 cytoarchitectonically distinct regions. One of these regions has indistinct borders from adjacent neostriatum. 2. HVc receives direct input from a small number of neurons in field L. 3. Areas adjacent to HVc received and send parallel projections to those of HVc.
Margoliash, D., E.S. Fortune, M. Sutter, C-H. Yu, D. Hardin, and A.Dave (1994) Distributed representation in the song system of oscines: evolutionary implications and functional consequences. Brain Behav. Evol. 44:247-264.
A review of thinking about song learning and production. It has been almost completely superceded by more recent results and reviews.
Margoliash, D. and E.. Fortune (1992) Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J. Neurosci., 12:4309-4326.
The most complex, both in the temporal and spectral domains, selectivities for acoustic signals in any animal system are described in this paper. These complex selectivities are produced by the song-learning process.
Fortune, E.S. and D. Margoliash (1992) Cytoarchitectonic organization and morphology of cells of the field L complex in adult male zebra finches (Taeniopygia guttata). J. Comp. Neurol., 325:388-404.
A detailed description of the anatomy of "field L" of the Nidopallium.


Abstracts:

Fortune, E.S. and G.J. Rose (2000) Voltage-dependent Na+ conductances in toral neurons enhance temporal filtering in Eigenmannia. Soc. Neurosci Abstr., 30:567.
Fortune, E.S. and G.J. Rose (1999) Frequency-dependent synaptic depression in the torus contributes to the AM filter of Eigenmannia. Soc. Neurosci Abstr, 29:550.
Rose, G.J. and E.S. Fortune (1996) Roles of adaptation, passive electrical filtering, and voltage-dependent conductances in the temporal selectivities of toral neurons. Soc. Neurosci. Abstr., 22:179.
Rose, G.J. and E.S. Fortune (1995) Parallels between the frequency filtering characteristics of ampullary neurons and the temporal filtering properties of tuberous neurons in the torus of Eigenmannia. Soc. Neurosci. Abstr., 21: 79.
Fortune, E.S. and D. Margoliash (1994) In vivo characterization of identified HVc neurons in the zebra finch. Soc. Neurosci. Abstr., 20: 74.
Fortune, E.S. and D. Margoliash (1992) Multiple auditory pathways into HVc. Soc. Neurosci. Abstr., 18:500.
Fortune, E.S. and D. Margoliash (1992) Neurons of the field L complex project directly into HVc. Proc. Third Int. Cong. Neuroethol., 345.
Fortune, E.S., and D. Margoliash. (1991) Thalamic input and cytoarchitecture of auditory neostriatum in zebra finch. Soc. Neurosci. Abstr. 17:446.
Fortune, E.S. and D. Margoliash (1989) Harmonic combination-sensitive neurons in the zebra finch. Soc. Neurosci. Abstr. 19:247.