The DiCaprio Lab
Neurobiology Program
Department of Biological Sciences
Ohio University
Integrative Properties of Nonspiking Neurons
My primary research focus is on the functional and integrative properties of nonspiking neurons involved in the control of motor behavior. The majority of neurons in most organisms must generate active, regenerative potentials (action potentials) in order to transmit information over even modest distances in the nervous system. In contrast, nonspiking neurons function without generating action potentials, and therefore use continuous or "analog" information transmission, rather than the requiring a "digital" encoding and transmission scheme inherent in the use of action potentials for information transmission and integration. Nonspiking neurons have been described in a variety of nervous systems and appear to play an important role in neuronal integration and provide a novel mechanism for the control of behavior.
A long standing project concerns the role of nonspiking neurons in the organization of neural networks which generate stereotyped motor behaviors. The network of neurons that coordinate precisely timed sequences of neural activity in order to produce coordinated movement are termed "central pattern generators" or CPGs. I have been using the ventilatory central pattern generator of the shore crab, Carcinus maenas, in these studies. Although the crab ventilatory system presents an interesting model for the investigation of CPG organization, the principal rationale for the development of this system is that it is almost exclusively composed of nonspiking neurons.
In the crab ventilatory system, nonspiking neurons are found at all levels
of the CPG, including frequency modulating
interneurons, CPG interneurons, sensory neurons and graded feedback from motor
neurons to the CPG. This work provides an opportunity to gain further insight
into the functional role of nonspiking local circuit interactions in a system
which is uniquely qualified for this investigation.
The recording at the left is from an isolated ganglion of the crab nervous
system. The top three traces (LEV, DEP and D2a+LEV) are extracellular
recordings from the nerves to the gill bailer and the lower two traces are
intracellular recordings from a ventilatory motor neuron innervating depressor
muscle D2a and a nonspiking interneuron, CPGi6 which is one of eight nonspiking
interneurons in the ventilatory CPG. The amplitude of the membrane potential
oscillation in CPGi6 is 35 mV. [Hit the "STOP" button on your
browser to halt the animation; "RELOAD" to play it again.]
Comparison of Nonspiking and Spiking Neurons: "Analog" vs. "Digital" Transmission in the Nervous System
We are also working on a project that allows a direct comparison of the
information processing capabilities of nonspiking and spiking neurons in a
sensorimotor system. Although nonspiking transmission has been investigated in
various systems, the assessment of the functional advantages of nonspiking
transmission has been hampered by the absence of an appropriate context for the
evaluation of these systems. We are determining the transfer functions
(input/output relationship) of nonspiking and spiking proprioceptors in the
first two joints of the crab leg and for the synapses and motor reflexes
associated with these receptors. The basal leg joint in the crab is monitored
by a single proprioceptor, the TCMRO, that contains two nonspiking and one
spiking neuron. The position, velocity and acceleration of the next most distal
joint is monitored by a single spiking receptor, the CB chordotonal organ, and
two nonspiking elastic strand receptors. One therefore has a system that
permits a direct comparison of these two distinct modes of information
transmission, although the physiological functions of the receptors are very similar
as are the motor behaviors that they mediate. The experimental approach employs
standard electrophysiological techniques and linear and nonlinear (Wiener
kernel) systems analysis methods in order to characterize the transfer function
of these proprioceptors. The Wiener approach utilizes Gaussian white noise as a
test stimulus to the system under study and determines a series of filters
(kernels) that describe both the linear and nonlinear characteristics of the
system. As the experimental preparation permits access to the reflex pathways
mediated by these receptors, the systems analysis approach will be extended to
investigate overall transfer properties of the synapses and motor reflexes in
response to sensory input from nonspiking and spiking receptors. An additional
goal is the determination of the magnitude and fidelity of information
transmission in nonspiking and spiking afferents using information theoretic
methods that have recently been applied to neuronal systems. Preliminary
results show that, over a frequency bandwidth of 200 Hz, the nonspiking
afferents transmit information at up to 2600 bits while the spiking afferents
of the CBCTO are capable of rates of ~150-250 bits/s.
Neural Control of Locomotion
I have been
collaborating with Dr. Ansgar Büschges and his laboratory
at the University of Cologne in several studies of the role of sensory input in
the control of locomotion.
In vertebrate and invertebrate walking, the motor pattern driving individual
legs results from the interaction between centrally generated commands,
feedback signals from sense organs, as well as coordinating signals from other
legs. Changes in load, information from joint proprioceptors and information on
the step phase of adjacent legs all strongly influence the motor pattern of
each individual leg. The generation of a functional walking motor pattern in a
multi-jointed limb also relies on coordination between movements of adjacent
leg joints. In the stick insect, individual joint oscillators form the basis
for motor patterning and we have been investigating several aspects of the role
of sensory signals in interjoint coordination. Recent collaborative projects have
focused on the of phasic and tonic proprioceptive information from specific leg
joints in patterning of the motor pattern off adjacent leg joints. Similarly,
we have started to investigate how coordinating signals from the neighboring
legs are processed in the local neuronal networks controlling the activity of
individual leg joints.
Post Doc
Recent and Selected Publications
DiCaprio,
Ralph A. (2004) Information Transfer
Rate of Nonspiking Afferent Neurons in the Crab. J. Neurophysiol. 92: 302-310.
Ansgar Buschges, A., Bjorn C. Ludwar, Dirk
Bucher, Joachim Schmidt, and Ralph A. DiCaprio (2004) Synaptic drive contributing to rhythmic activation of motoneurons in the
deafferented stick insect walking system. Eur. J. Neurosci. 19: 1856-1862.
Hooper, S. L. and R. A. DiCaprio (2004) Crustacean Motor Pattern Generator Networks. Neuro-Signals 13(1,2): 50-69.
Gamble, E. Rolland and Ralph A. DiCaprio. (2003) Nonspiking and Spiking Proprioceptors in the Crab: White Noise Analysis of Spiking CB-Chordotonal Organ Afferents. J Neurophysiol. 89: 1815-1825.
DiCaprio, Ralph A. (2003) Nonspiking and Spiking Proprioceptors in the Crab: Nonlinear Analysis of Nonspiking TCMRO Afferents. J Neurophysiol. 89: 1826-1836.
Bucher, Dirk, Turgay Akay, Ralph A. DiCaprio and Ansgar Buschges (2003) Interjoint coordination in the stick insect leg-control system: The role of positional signaling. J Neurophysiol. 89: 1245-1255.
DiCaprio, Ralph A., Harald Wolf and Ansgar Buschges (2002) Activity-dependent sensitivity of proprioceptive sensory neurons in the stick insect femoral chordotonal organ. J. Neurophysiol. 88: 2387-2398.
Ridgel, A.L., Frazier, S.F., DiCaprio, R.A. and S.N. Zill. (2000) Encoding forces in posture and locomotion: Static and dynamic responses of cockroach tibial campaniform sensilla. J. Comp. Physiol. 186: 359-374.
DiCaprio, R.A. (1999) Gating of afferent input by a central pattern generator.
J. Neurophysiol. 81: 950-953. 
Full text of this
paper.
Ridgell, A.L., Frazier, S.F., DiCaprio, R.A. and S.N. Zill. (1999) Active
signaling of leg loading and unloading in the cockroach. J. Neurophysiol. 81:
1438-1442. Full text of this paper.
DiCaprio, R.A. (1997) Plateau potentials in motor neurons in the crab ventilatory
system. J. exp. Biol 200(12): 1725-1736. Full text of this
paper.
DiCaprio, R.A., Jordan, G. and T. Hampton. (1997) Maintenance of motor
pattern phase relationships in the ventilatory system of the crab. J. Exp.
Biol. 200(6): 963-974. Full text of this paper.
El Manira, A., Cattaert, D., Wallen, P., DiCaprio, R.A. and F. Clarac. (1993) Electrical coupling of mechanoreceptor afferents in the crayfish: A possible mechanism for enhancement of sensory signal transmission. J. Neurophysiology 69(6): 2248-2251.
El Manira, A., DiCaprio, R.A., Cattaert, D. and F. Clarac (1991). Monosynaptic interjoint reflex and its central modulation during fictive locomotion in the crayfish. Eur. J. Neurosci. 3: 1219-1231.
DiCaprio, R.A. (1990) An interneurone mediating motor programme switching in the ventilatory system of the crab. J. Exp. Biol. 154: 517-535.
DiCaprio, R.A. (1989) Nonspiking interneurons in the central pattern generator for ventilation in the crab. J. Comp. Neurol. 265: 82-106.
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DiCaprio's favorite recreational activity