Commissural and Perforant Path Interactions in the Rat Hippocampus Field Potentials and Unitary Activity

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Commissural and Perforant Path Interactions in the Rat Hippocampus Field Potentials and Unitary Activity Exp Brain Res (1981) 43:429-438 Springer-Verlag 1981 Commissural and Perforant Path Interactions in the Rat Hippocampus Field Potentials and Unitary Activity G. Buzs~iki 1 and G. Cz6h 2 ~Department of Physiologyand 2Department of Biophysics, University Medical School, H-7643 P6cs, Hungary Summary. The interaction of the commissural and path which traverses the hippocampal fissure and perforant path systems was studied by recording makes synaptic contacts with the granule cells of the extracellular field potentials and single unit activity in dentate gyrus as well as with the pyramidal cells of the dentate gyrus in urethane-anesthetized rats. Con- CA 3-4 region (Ram6n y Cajal 1911; Lorente de N6 ditioning commissural volleys suppressed extracellu- 1934; Steward 1976). The axons of the granule cells lar synaptic potentials, population spikes and single (mossy fibers) travel through the hilus of the dentate unit discharges evoked by perforant path stimulation. fascia and form giant synapses with the pyramidal Commissural stimulation (single or repetitive) failed neurons of CA 3-4 region. The latter cells give rise to to induce a population spike, however strong the axons which leave the hippocampus, and in addition, stimulation. About half of the cells fired monosynap- terminate in the stratum radiatum of the ipsilateral tically to perforant path volleys and 20% to commis- CA i region by way of the Schaffer collateral system. sural volleys. Half of the commissurally driven units The major physiological characteristics of this fired before or coincided with field potential onset. trisynaptic circuit have already been elucidated The antidromic mechanism of these short latency (Andersen et al. 1966a, b, 1971a; L0mo 1971a, bi unitary spikes was shown by the collision test. Winson and Abzug 1977). Much less research has Commisural activation reduced spontaneous cell fir- been devoted to the physiological properties of the ing without previous excitation in 25% of the commissural pathways (Deadwyler et al. 1975a; neurons. Less than 6% of the cells responded to Segal 1977, 1978; Steward et al. 1977; Buzs~iki 1980). stimulation of both inputs, indicating little conver- The commissural fibers originate in the CA 3-4 gence between the two pathways. We contend that a region of the hippocampus and terminate in the inner simple form of recurrent inhibition fails to explain third of the molecular layer of the dentate gyms, in the above findings, and the possibility of feed- the stratum radiatum, and, to a lesser extent, in the forward inhibition by commissural activation has stratum oriens of fields CA 1 and CA 3 of the been raised. contralateral hippocampus (Blackstad 1956; Raisman et al. 1965; Laatsch and Cowan 1967; Gottlieb and Key words: Hippocampus - Feed-forward inhibition Cowan 1973; Hjorth-Simonsen and Laurberg 1977; - Commissural and perforant path inputs - Field potentials - Unit activity Fricke and Cowan 1978; Swanson et al. 1978). The purpose of the present investigation was to study the functional characteristics of the commis- It is apparent that a thorough understanding of the sural system and its interaction with the perforant physiological properties and interactions of the path system in the dentate gyrus. A preliminary numerous hippocampal afferent systems (Chronister report has appeared elsewhere (Buzsgtki et al. 1979). and White 1975; MacLean 1975) is a prerequisite for our understanding of hippocampal functioning. The Methods two major afferent systems to the hippocampus are the perforant and commissural pathways. Axons Surgical Procedure from cells of the entorhinal area form the perforant Thirty male, mature hooded rats (250-350 g) were anesthetized Offprint requests to: Dr. Gy6rgyBuzsfiki (address see above) with urethane (1.5 g/kg, i.p.). Teflon-coatedstainless-steel, twisted 0014-4819/81/0043/0429/$ 2.00 430 G. Buzs~iki and G. Czrh: Interactions of Hippocampal Inputs bipolar electrodes (100 ~tm in diameter, with intertip distances of Results less than 0.5 mm) were implanted in the CA 3-4 region of the left dorsal hippocampus (3.0 mm posterior to bregma, 3.2 mm lateral to midline and 3.6 mm below the brain surface). An additional pair Field Responses of electrodes was placed in the right angular bundle (AP = 7.0 ram, L = 4.5 ram, V = -4.5 mm) to stimulate perforant path Responses to perforant path and commissural stimu- fibers. The electrodes were fixed with dental cement. A hole was lations were found similar in all major respects as drilled over the right hippocampus and the dura mater was cut previously reported by others (Andersen et al. 1966a, under a dissection microscope. b; 1971a; LOmo 1971a, b; Deadwyler et al. 1975a; McNaughton and Barnes 1977; Steward et al. 1977), and will not be reiterated here. Some comments are Recording and Stimulation Procedures in order, however. Stimulation of the contralateral CA 3-4 field of Recording was made with either glass micropipettes (2 M NaCI, the hippocampus elicited short latency evoked poten- 2-20 M~) or tungsten microelectrodes (2-5 ~tm tip, 5-15 M~?). Pilot experiments indicated that high impedance of the recording tials from both field CA 1 and dentate gyrus. When electrode was a prerequisite for isolating neurons in the granular strong commissural volleys were used, a large popu- layer. An indifferent electrode was placed in the neck muscles. lation spike appeared on the initial deflection of the Amplification, oscillographic display and photography were con- extracellular synaptic wave in the CA 1 pyramidal ventional. The amplifier had a flat frequency response from d.c. to layer. On further penetration by the recording elec- 5,000 Hz. Occasionally the bioelectric data were recorded on FM tape for subsequent analysis. The stimulating pulses were mono- trode, the amplitude of the population spike progres- phasic square waves (0.1 ms 2-100 V), delivered at a rate of sively decreased and fell to zero as the electrode 0.1-0.2 Hz. For certain tests the rate was increased from 2 to traversed the dentate gyms. 100 Hz. Stimulation of the contralateral CA 3-4 region failed to evoke population spikes in the dentate area even at intensities which produced afterdischarges. Histology Repetitive impulses were also ineffective. Because it has been thought that this lack of commissurally Following each experiment, d.c. current was passed through the evoked population spikes in the dentate area may be stimulating electrodes. The glass microelectrode was cut just due to a decreased effectiveness in synchronously below the shank and left in the brain. In experiments utilizing tungsten electrodes, tip locations were marked by passing a d.c. exciting and discharging a large number of granule current (5-10 ~A, 5 s) through the electrodes. The subjects were cells (see Discussion), the flollowing experiment was perfused with saline, 3% potassium ferrocyanide (blue spot carried out. The strength of the perforant path reaction) and formalin. The brains were excised and imbedded in volleys was adjusted slightly above population spike paraffin. Coronal sections were stained with cresyl violet. threshold and then commissural stimulation was increased to supramaximal values. With this proce- dure, in some instances, the commissurally evoked Data Analysis field response was higher in amplitude than the perforant path evoked synaptic potential at any point Bioelectric activity of the hippocampus was sampled at 25-100 ~m along the recording track. This experiment showed steps to a depth of 4-5 mm below the surface of the cortex, 2.7 mm that commissural stimulation was not capable of lateral from the midsaggital suture and 3.0 mm posterior to the bregma. Field potentials and unitary activity were averaged by a discharging large numbers of neurons, although the Neurolog Averager (Digitimer). Unitary activity was collected in synaptic field potential was of greater amplitude than eight animals. Units were classified as theta ceils, complex spike that of the perforant path evoked response, which cells or other cells (Ranck 1973; Fox and Ranck 1981). Theta cells did produce a population spike (Fig. 1). were recognized by their short duration (< 0.5 ms), a rhythmic High frequency stimulation of the commissural firing which was phase-locked to the negative component of the EEG theta waves, and their invariable increase in frequency in path (50 Hz, 5 s) reduced the amplitude of the association with the appearance of theta activity. Theta activity dentate response to single volleys after the train. was induced by tail pinching or by eserin injection (1 mg/kg, i.v.). Recovery of the evoked field response seemed to A unit was classified as a complex spike cell if it produced a firing parallel the recovery of the EEG activity. During pattern as shown in Fig. 5A at least once. Cells which did not meet these criteria were classified as "other" cells. This third category is afterdischarges, the dentate field response was overestimated by the fact that not all units were held long enough reduced to zero or even reversed its polarity. On the to classify them as theta or complex spike cells. Latencies were other hand, high frequency stimulation of the com- determined by measuring the time interval defined by the onset of missural path resulted in long-term potentiation in shock artifact and some special aspect of the response. Short latency commissural units (see Results) were tested for antidromic the CA 1 region (Buzs~iki 1980). activation by measuring the refractory period, and attempting Strong commissural volleys sometimes generated collision (Fuller and Schlag 1976). a later evoked response following the primary G. Buzsfiki and G. Cz6h: Interactions of Hippocampal Inputs 431 A A 4 ms c PP ;: IL _ !! a W c pp V B B (.- C Pig. 1A, B. Comparison of commissural and perforant path evoked responses at different depths of the dentate gyrus. A molecular layer.
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