Correlation of electrophysiology, shape and synaptic properties of myenteric AH neurons of the guinea pig distal colon Kulmira Nurgali, John B. Furness * , Martin J. Stebbing Department of Anatomy and Cell Biology and Centre for Neuroscience, University of Melbourne, Parkville, Victoria 3010, Australia Received 8 May 2002; received in revised form 29 August 2002; accepted 4 September 2002 Abstract Well-defined correlations between morphology, electrophysiological properties and the types of synaptic inputs received are established for myenteric neurons in the guinea pig ileum. However, in the distal colon, the correlations between AH electrophysiological properties, presence of fast excitatory post-synaptic potentials (EPSPs) and neuronal shape have been inadequately resolved and it is unknown whether any colon neurons receive synaptic inputs that generate sustained excitation. In this work, we have used intracellular recording, dye filling via the recording electrode, and immunohistochemistry to classify distal colon neurons. Neurons (24 of 168) had Dogiel type II morphology and 42% of these were dendritic type II neurons, compared to about 10% in the ileum. All Dogiel type II neurons had AH electrophysiological properties, including a prolonged post-spike after-hyperpolarization (AHP). None of these received fast excitatory post-synaptic potentials, 11 of 22 tested exhibited sustained slow post-synaptic excitation (SSPE) in response to 1 Hz pre-synaptic stimulation and 13 of 15 tested were immunoreactive for calbindin. Neurons (127) had Dogiel type I, filamentous or other uniaxonal cell shape and S type electrophysiology. Neurons of this group had fast excitatory post-synaptic responses to stimulation of synaptic inputs, but did not exhibit a prolonged post-spike after-hyperpolarization or sustained slow post-synaptic excitation. Another group of neurons (17) had both AH electrophysiological characteristics and fast excitatory post-synaptic potentials. These neurons had Dogiel type I, filamentous or other uniaxonal shapes, but none had Dogiel type II morphology and none showed sustained slow post-synaptic excitation. It is concluded that Dogiel type II neurons are all AH neurons and are probably intrinsic sensory neurons that could be involved in long- term changes in excitability in the colon. All other neurons are monoaxonal; these are motor neurons and interneurons, and most are S neurons, electrophysiologically. A small number of monoaxonal neurons display AH electrophysiology and also receive fast excitatory synaptic inputs. These include motor and interneurons, but not sensory neurons. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Enteric nervous system; Synaptic transmission; Sensory neurons; Neuron morphology 1. Introduction There has been steady progress in defining the types of neurons in the enteric nervous system and their places in enteric nerve circuits. A significant advance was to combine electrophysiological characterization with morphology and chemistry by using marker dyes to fill neurons that had been recorded from and subsequently to examine their shapes and immunohistochemical labelling (Hodgkiss and Lees, 1983; Bornstein et al., 1984; Iyer et al., 1988; Messenger et al., 1994; Clerc et al., 1998; Lomax et al., 1999; Tamura et al., 2001). Morphological classification of enteric neurons is based on the 1899 system of Dogiel (1899). One of the types he defined, neurons with large smooth-surfaced oval cell bodies and several long processes, are known as Dogiel type II neurons. In the guinea pig small intestine, these neurons are well defined by a number of electrophysiological and chem- ical features. They have AH electrophysiological character- istics (Iyer et al., 1988; Clerc et al., 1998). That is, they have broad action potentials that are partly tetrodotoxin resistant, and they have prolonged after-hyperpolarizations (late AHPs) following single soma action potentials. In the ileum, these neurons very rarely exhibit fast excitatory post-synap- tic potentials (EPSPs), and, when they are observed, fast EPSPs are of small amplitude (Hirst et al., 1974; Iyer et al., 1988; Lees et al., 1992; Bornstein et al., 1994; Evans et al., 1994; Song et al., 1997). Stimulation of interganglionic 1566-0702/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII:S1566-0702(02)00212-6 * Corresponding author. Tel.: +61-3-83448859; fax: +61-3-93475219. E-mail address: j.furness@unimelb.edu.au (J.B. Furness). www.elsevier.com/locate/autneu Autonomic Neuroscience: Basic and Clinical 103 (2003) 50 – 64