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Organization of cat striate cortex: a correlation of receptive-field properties with afferent and efferent connections.

The purposes of this study were 1) to relate the receptive-field characteristics of area 17 cells to their afferent and efferent connections, and 2) to obtain quantitative data from area 17 neurons for later comparison with area 18 cells. Intra- and extracellular recordings were obtained in paralyzed preparations which were anesthetized with nitrous oxide. The connectivities of the recorded cells were determined from responses to electrical stimulation of afferent and efferent pathways. In parallel to the classification of units as simple and complex cells, the receptive fields were grouped in four classes according to the spatial arrangement of on- and off-areas; class I, fields with exclusive on- or off-areas; class II, fields with spatially separate on- and off-areas; class III, fields with mixed on-off areas; class IV, fields which could not be mapped with stationary stimuli. The results from electrical stimulation suggest two major classes of cells: cells in the first group are driven mainly or exclusively by LGN afferents. They rarely receive additional excitation from intrinsic or callosal afferents and rarely possess corticofugal axons. Cells in the second group receive either converging inputs from LGN afferents and further intrinsic afferents or only from intrinsic afferents. They frequently received additional input from callosum and from recurrent collaterals of corticofugal axons. They project subcortically more often than cells in the first group. Cells in both groups can be driven either by X- or Y-type afferents. Cells in the first group have mainly class I and class II fields or simple fields, whereas the neurons in the second group have mainly class III and class IV fields or complex fields. Thus, simple and complex cells differ in their connectivity patterns, but the discriminative parameter is neither the selective connection to the X- or the Y-system nor, in a strict sense, the synaptic distance from subcortical input. From the combined consideration of receptive-field properties and connectivity patterns it is concluded that class I and class II cells or simple cells are concerned mainly with the primary analysis of subcortical activity, whereas class III and class IV cells or complex cells perform a correlative analysis between highly convergent activity from extrinsic and intrinsic afferents.

Animals↗

Relative strength of synaptic input from short-latency pathways to motor units of defined type in cat medial gastrocnemius.

1. Intracellular recording and stimulation techniques were used in anesthetized cats to study the interrelations between amplitudes of PSPs produced by electrical stimulation of several short-latency pathways to MG alpha motoneurons and the mechanical properties of muscle units innervated by the same cells. Motor-unit types were identified by muscle-unit properties.2. The maximum amplitudes of monosynaptic EPSPs produced in MG motoneurons by activation of homonymous (MG) and heteronymous (LGS) group Ia afferents were clearly related to motor-unit type, being, on the average, largest in type S units, somewhat smaller in type FR and F(int) units, and smallest in type FF units. Correspondingly, group Ia EPSP amplitudes were inversely correlated with muscle-unit tension production and directly correlated with resistance to fatigue. The same input distribution was true for disynaptic IPSPs produced by group Ia afferents from antagonist ankle flexors.3. The amplitudes of monosynaptic EPSPs produced by fibers descending in the ipsilateral ventral funiculi of the low thoracic cord were not clearly related to MG motor-unit type or (therefore) to muscle-unit properties.4. A quantitative input-output model of the MG motor-unit pool, based in part on the present results, suggests that overall characteristics of MG motor units, and their relative numbers in the MG pool, reflect functional specializations determined by specific mechanical demands placed on the MG muscle by the usual motor behavior of the animal.

Animals↗

Functional organization of vestibular and visual inputs to neck and forelimb motoneurons in the frog.

1. Intracellular responses in neck and forelimb motoneurons to electrical stimulation of the vestibular nerve, the optic tectum, and the optic nerve were studied in frog. 2. Stimulation of the anterior branch of the vestibular nerve typically produced EPSPs, bilaterally, in neck, shoulder (DOR), and forelimb extensor (TRI, RAD) motoneurons, and bilateral IPSPs in forelimb adductor (PED) and flexor (ULN, COR) motoneurons. 3. Latencies of PSPs recorded in neck, shoulder, and proximal extensor motoneurons (TRI) were mostly in the disynaptic range, whereas many of those recorded in distal extensor (RAD) and in adductor and flexor motoneurons involved three synapses. 4. Lesion of the vestibulospinal fibers greatly reduced the vestibular nerve-evoked field potentials in the spinal cord and the occurrence of PSPs in forelimb motoneurons. These results as well as the latency measurements suggest that the pathway linking vestibular nerve and forelimb motoneurons mainly consists of vestibulospinal fibers, though involvement of other structures for production of later PSPs could not be completely ruled out. Hemisection of the brain stem at its most caudal level showed that the pathway to the contralateral motoneurons crosses at the level of brain stem as well as in the spinal cord. 5. Stimulation of the optic tectum produced EPSPs, IPSPs, and a mixture of EPSPs and IPSPs in neck, shoulder, and forelimb motoneurons, bilaterally. Most frequently, a combination of an excitation and inhibition was observed. The pathway from the optic tectum to neck and limb motoneurons is at least dysnaptic in nature. 6. Stimulation of the optic nerve produced IPSPs and a mixture of EPSPs and IPSPs in neck and forelimb motoneurons. Impulses originating from the optic nerve descend as far as to lumbar motoneurons producing EPSP-IPSP sequences bilaterally. 7. Interaction studies suggested that the vestibular and optic pathways to neck and forelimb motoneurons are separate from each other so that the site of integration of vestibular and visual input occurs at the level of motoneurons. 8. Evidence for electronic coupling among forelimb motoneurons and electrical synaptic transmission in th pathway linking vestibular nerve and forelimb motoneurons is presented.

Animals↗

Aplysia bursting neurons as endogenous oscillators. I. Phase-response curves for pulsed inhibitory synaptic input.

1. The left upper quadrant bursting neurons in the abdominal ganglion of Aplysia are isochronous, nonlinear oscillators. Transmembrane current and temperature are parameters of the bursting oscillator. 2. The phase-response curve (PRC) for pulsed inhibitory synaptic input from an interneuron describes the phase shift produced by synaptic input at different phases of the burst cycle. 3. The characteristic shape of the PRC consists of two linear functions that intersect at the point in the cycle where the burst of spikes ends. Whether the net effect of the synaptic input at a given phase is phase advance or phase delay depends on 1) the number of spikes inhibited, and 2) the duration of the inhibition relative to the duration of the free-run period. 4. The shape of the PRC remains constant when a stepwise change in a parameter is introduced, when the duration of the synaptic input is increased, when the fast component of the IPSP is blocked, and when a long hyperpolarizing pulse is used to mimic the slow IPSP. 5. The shape of the PRC is changed when short hyperpolarizing pulses or antidromic action potentials are used and when only the pacemaker oscillation is present in the bursting neuron. 6. Therefore, the synaptic modulation of the bursting rhythm is determined by the voltage change produced by the IPSP and its inhibition of spikes in the bursting neuron.

Action Potentials↗

A determination of excitability changes in dorsal spinocerebellar tract neurons from spike-train analysis.

1. Responses of DSCT neurons to random electrical stimulation of peripheral nerves of the hindleg at group I intensity were studied using cross-correlation analysis of the output spike train with the stimulus. Three types of response were found: type 1 was due to monosynaptic activation of DSCT cells, type 2 resulted from inhibition of those cells, and type 3 was due to a long-latency excitation that was probably polysynaptic. 2. Most of the units studied responded to stimulation of both proximal and distal flexor and extensor nerves. The extensive convergence of afferent input on DSCT cells is much greater than has been observed previously, with type 2 and type 3 responses totaling 80% of the observed responses. We attribute this to the sensitivity of the analysis in detecting small changes in postsynaptic excitability. 3. The results of the study, particularly the derivation of postsynaptic excitability changes, generally confirm those of earlier work employing intracellular recording. 4. By varying stimulus rate and stimulus intensity in the group 1 range and simulating the resulting correlations, we conclude that excitability changes in DSCT cells are the net result of complex interactions involving excitation and inhibition. A summary of these findings is presented as a model for the minimum circuitry necessary to account for the observed behavior.

Afferent Pathways↗

Primary afferent depolarization and inhibory interactions in spinal cord of the stingray, Dasyatis sabina.

1. Excitability changes in primary afferents and inhibitory interactions in evoked spinal cord activity were investigated in unanesthetized stingrays (Dasyatis subina) with high cervical spinal transections. 2. Primary afferent excitability increases following a conditioning stimulus to an adjacent segmental nerve were demonstrated with the Wall (31) technique. 3. Stimulation of A-alpha,beta and A-delta afferent fibers produced excitability increases in both A-alpha,beta and delta-fibers of the adjacent segment. 4. The excitability increase had a latency of about 10 ms, it peaked around 25 ms, and the change lasted more than 100 ms. 5. The central afferent volley in A-alpha,beta fibers and the N1- and late negative waves due to postsynaptic activity of dorsal horn interneurons were reduced by conditioning volleys in adjacent afferent nerves. The time course of the inhibition paralleled that of the excitability increases in afferent terminal arborizations, suggesting that the depression of postsynaptic activity is, at least in part, due to presynaptic inhibition. 6. Reduction of evoked discharges and excitatory postsynaptic potentials was observed in recordings from interneurons with a time course similar to that of the primary afferent depolarization (PAD). 7. Conditioning volleys in afferents of adjacent peripheral nerves produced facilitation or inhibition of segmental reflexes.

Afferent Pathways↗

Discharge properties of pontine reticulospinal neurons during sleep-waking cycle.

1. Reticulospinal neurons were identified by antidromic invasion from spinal cord electrodes chronically implanted at C4 in cats. 2. Most of the neuronal population studied lay within the medial portion of the giant cell field from the anterior pontine and to the anterior medullary reticular formation (FTG). A few cells were found in the tegmental reticular nucleus (TRC) which has not previously been known to project to the spinal cord. 3. Extracellular action potentials from the neuronal somata of the identified neurons were recorded continuously throughout naturally occurring sleep-waking cycles. 4. The identified reticulospinal neurons shared three properties, suggesting a generator function in desynchronized sleep (D) (with previously recorded but unidentified FTG neurons): selectivity (or concentration of discharge in D); tonic latency (or firing rate increases beginning several minutes prior to D); and phasic latency (or firing rate increases occurring prior to eye movements within D). 5. The location, discharge properties, and spinal projections of FTG neurons are, thus, all consistent with the hypothesis that they may directly mediate some of the descending excitatory and inhibitory influences on spinal reflex pathways in desynchronized sleep.

Animals↗