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 the ventilatory motor pattern recorded
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.
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 applied to this neuronal system. Over a frequency
bandwidth of 200 Hz,
the
nonspiking afferents transmit information at up to 2600 bits/sec while
the
spiking
afferents of the CBCTO are capable of rates of ~150-250 bits/sec.
Neural Control of Locomotion
I have been
collaborating with Dr. Ansgar Büschges and his laboratory
at the
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.
Recent and Selected Publications
DiCaprio, Ralph A., Cyrus P. Billimoria, and Björn Ch. Ludwar. (2007) Information rate and spike-timing precision of proprioceptive afferents J Neurophysiol 98: 1706–1717.
Büschges,
A. and R.A. DiCaprio. (2007) Somatosensation
in Invertebrates, in The Senses: A Comprehensive Reference, J.
Kaas,
ed., V 5.18, Elsevier, Oxford, UK.
Billimoria,
Cyrus P., Ralph A. DiCaprio, John T.
Birmingham, L.F. Abbott and Eve Marder.
(2006) Modulation of spike-timing precision in sensory neurons.
J.
Neurosci. 26: 5910-5919.PDF file
DiCaprio,
Ralph A. (2004) Information
Transfer Rate of Nonspiking Afferent Neurons in the Crab. J.
Neurophysiol. 92:
302-310. PDF file
Ansgar
Büschges, A.,
Björn 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. PDF file
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. PDF file
Bucher, Dirk, Turgay Akay, Ralph A. DiCaprio and Ansgar Büschges (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 Büschges (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. PDF file
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
DiCaprio, R.A. (1997) Plateau potentials in motor neurons in the
crab
ventilatory system. J. exp. Biol 200(12): 1725-1736. Full
text.
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.
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.
For further
information, e-mail to DiCaprio
DiCaprio's favorite recreational
activity 