Sequential activation of microcircuits underlying somatosensory-evoked potentials in rat neocortex.

Evoked cortical field potentials are widely used in neurophysiological studies into cortical functioning, but insight in the underlying neural mechanisms is severely hampered by ambiguities in the interpretation of the field potentials. The present study aimed at identifying the precise relationships between the primary evoked cortical field potential (the positive-negative [P1-N1]response) and the temporal and spatial sequence in which different local cortical micro-circuits are recruited. We electrically stimulated the median nerve and recorded field potentials using a 12-channel depth probe in somatosensory cortex of ketamine anesthetized rats. Current source density analysis was used and a grand average was constructed based on all individual animals taking into account individual differences in cortical layering. Manipulation of stimulus strength, selective averaging of single trial responses, and double-pulse stimulation, were used to help disentangle overlapping dipoles and to determine the sequence of neuronal events. We discriminated three phases in the generation of the P1-N1 wave. In the first phase, specific thalamic afferents depolarize both layer III and layer V pyramidal cells. In the second phase, superficial pyramidal cells are depolarized via supragranular intracortical projections. In the third phase, population spikes are generated in layer Vb pyramidal cells, associated with a distinct fast (approximately 1 ms) sink/source configuration. Axon-collaterals of layer Vb pyramidal cells produce an enhanced activation of the supragranular pyramidal cells in layer I-II, which generates N1.

Neuronal representation of disappearing and hidden objects in temporal cortex of the macaque.

Neurons in the anterior regions of the banks of the superior temporal sulcus (STSa) of the macaque monkey respond to the sight of biologically significant stimuli such as faces, bodies and their motion. In this study the responses of STSa neurons were recorded during the gradual occlusion of the experimenter and other mobile objects behind screens at distances of 0.5-4 m from the monkeys. The experimenter or other object remained out of sight for 3-15 s before emerging back in to view. We describe a population of neurons (n=33) showing increased activity during the occlusion of objects that was maintained for up to 11 s following complete occlusion (when only the occluder itself was visible). This increase in activity was selective for the position of the occlusion within the testing room. Many neurons showed little or no change in activity prior to occlusion when the object or experimenter was completely in view. By coding for the presence and location of recently occluded objects, these responses may contribute to the perceptual capacity for object permanence.

Neural representation for the perception of the intentionality of actions.

A novel population of cells is described, located in the anterior part of the superior temporal sulcus (STSa, sometimes called STPa) of the temporal lobe in the macaque monkey. These cells respond selectively to the sight of reaching but only when the agent performing the action is seen to be attending to the target position of the reaching. We describe how such conditional selectivity can be generated from the properties of distinct cell populations within STSa. One cell population responds selectively to faces, eye gaze, and body posture, and we argue that subsets of these cells code for the direction of attention of others. A second cell population is selectively responsive to limb movement in certain directions (e.g., responding to an arm movement to the left but not to an equivalent leg movement or vice versa). The responses of a subset of cells sensitive to limb movement are modulated by the direction of attention (indicated by head and body posture of the agent performing the action). We conclude that this combined analysis of direction of attention and body movements supports the detection of intentional actions.

Effect of image orientation and size on object recognition: responses of single units in the macaque monkey temporal cortex.

This study examined how cells in the temporal cortex code orientation and size of a complex object. The study focused on cells selectively responsive to the sight of the head and body but unresponsive to control stimuli. The majority of cells tested (19/26, 73%) were selectively responsive to a particular orientation in the picture plane of the static whole body stimulus, 7/26 cells showed generalisation responding to all orientations (three cells with orientation tuning superimposed on a generalised response). Of all cells sensitive to orientation, the majority (15/22, 68%) were tuned to the upright image. The majority of cells tested (81%, 13/16) were selective for stimulus size. The remaining cells (3/16) showed generalisation across four-fold decrease in size from life-sized. All size-sensitive cells were tuned to life-sized stimuli with decreasing responses to stimuli reduced from life-size. These results do not support previous suggestions that cells responsive to the head and body are selective to view but generalise across orientation and size. Here, extensive selectivity for size and orientation is reported. It is suggested that object orientation and size-specific responses might be pooled to obtain cell responses that generalise across size and orientation. The results suggest that experience affects neuronal coding of objects in that cells become tuned to views, orientation, and image sizes that are commonly experienced. Models of object recognition are discussed.

Central and peripheral control of the trigger mechanism for kicking and jumping in the locust.

A crucial stage of the locust kick motor program is the trigger activity that inhibits the flexor motorneurons at the end of flexor-extensor coactivation and releases the tibia. One source of this inhibition is the M interneuron, which produces a spike burst at the time of the trigger activity. Previous work has suggested that sensory input resulting from extensor muscle tension may contribute to the M spike burst. We find that extensor muscle tension produced during thrusting behavior or by direct electrical stimulation with the tibia held fixed results in the depolarization of M, but this is not of sufficient amplitude to account for the M spike burst during the trigger activity. Furthermore, M still produces a spike burst after ablating the sensory systems that produce the response to the muscle stimulation. It is concluded that the major component of the M trigger activity is central in origin, although sensory feedback from extensor muscle tension makes some contribution. The combination of both central and peripheral paths for M activation may enhance the robustness of the behavior.

The concerted activity in parallel proprioceptive pathways controls the initiation of co-activation in the locust kick motor programme.

To jump and kick the locust uses a catapult mechanism implemented by a three-stage motor programme: initial flexion of the hind tibiae, co-activation of the antagonist flexor and extensor tibiae motor neurons and trigger inhibition of the flexor motorneurons. The transition from stage 1 to stage 2 thus involves a switch from the normal alternate activation to co-activation of the antagonist tibrae motorneurons. However, co-activation has never been observed when the central nervous system has been isolated from the leg. This led us to investigate the possibility that the transition from stage 1 to stage 2 is controlled by a proprioceptive signal. In the first set of experiments intracellular recordings were made in the flexor and extensor motorneurons while the position of the tendon of the femoral chordotonal organ (FCO), which signals tibial position and movement, was experimentally controlled. In these heavily dissected preparations, stretch of the FCO tendon (signalling tibial flexion) was a necessary condition for co-activation. However, in minimally dissected preparations (in which merely EMG recordings were made), we found that co-activation occurred even when the FCO was signalling tibial extension, suggesting the involvement of other proprioceptors. A series of experiments were then conducted on minimally dissected preparations to determine the relative contributions of each of the three main hind leg proprioceptors which might signal tibial flexion: the FCO, the lump receptor and Brünners organ. When all three proprioceptors were intact the chance of evoking co-activation was largest, when all three were eliminated co-activation could no longer be evoked, irrespective of the level of arousal. Various combinations of partial de-afferentation showed that the FCO plays the major role, with the lump receptor and Bünners organ playing significant, but progressively less important, roles. We conclude that the three receptors act together as a permissive proprioceptive gate for the kick and jump motor programme, but with a hierarchy of the strengths of their effectiveness.

The influence of proprioceptors signalling tibial position and movement on the kick motor programme in the locust

Four main proprioceptors monitor tibial position in the hindleg of the locust: the femoral chordotonal organ (FCO), the lump receptor, the suspensory ligament receptors and Brunner's organ. The influence of these proprioceptors on quantitative aspects of the kick motor programme has been investigated. The parameters measured were the duration of the initial flexion burst, the duration of co-activation of flexor and fast extensor tibiae (FETi) motoneurones, the number of FETi spikes during the co-activation, the interval between the kick and post-kick flexion, the number of FETi spikes occurring in this interval and the duration of post-kick flexion activity. The lump receptor and Brunner's organ have no detectable effect on any of these parameters. The FCO has highly significant effects on the duration of both initial flexion and post-kick flexion bursts, and on the number of FETi spikes occurring after the moment of tibial extension. The suspensory ligament receptors have significant effects upon the number of FETi spikes after the kick and the interval between the kick and the post-kick flexion. However, no proprioceptor had any influence upon the duration of co-activation or the number of FETi spikes during the co-activation. Thus, although elements of the kick motor programme preceding and following co-activation are strongly influenced by proprioceptors monitoring tibial position and movement, the co-activation stage, which is central to the effectiveness of the complete behaviour pattern, is not affected.

Peripheral control of the gain of a central synaptic connection between antagonistic motor neurones in the locust

The metathoracic fast extensor tibiae (FETi) motor neurone of locusts is unusual amongst insect motor neurones because it makes output connections within the central nervous system as well as in the periphery. It makes excitatory chemical synaptic connections to most if not all of the antagonist flexor tibiae motor neurones. The gain of the FETi-flexor connection is dependent on the peripheral conditions at the time of the FETi spike. This dependency has two aspects. First, sensory input resulting from the extensor muscle contraction can sum with the central excitatory postsynaptic potential (EPSP) to augment its falling phase if the tibia is restrained in the flexed position (initiating a tension-dependent reflex) or is free to extend (initiating a movement-dependent resistance reflex). This effect is thus due to simple postsynaptic summation of the central EPSP with peripheral sensory input. Second, the static tibial position at the time of the FETi spike can change the amplitude of the central EPSP, in the absence of any extensor muscle contraction. The EPSP can be up to 30 % greater in amplitude if FETi spikes with the tibia held flexed rather than extended. The primary sense organ mediating this effect is the femoral chordotonal organ. Evidence is presented suggesting that the mechanism underlying this change in gain may be specifically localised to the FETi-flexor connection, rather than being due to general position-dependent sensory feedback summing with the EPSP. The change in the amplitude of the central EPSP is probably not caused by general postsynaptic summation with tonic sensory input, since a diminution in the amplitude of the central EPSP caused by tibial extension is often accompanied by overall tonic excitation of the flexor motor neurone. Small but significant changes in the peak amplitude of the FETi spike have a positive correlation with changes in the EPSP amplitude, suggesting a likely presynaptic component to the mechanism of gain control. The change in amplitude of the EPSP can alter its effectiveness in producing flexor motor output and, thus, has functional significance. The change serves to augment the effectiveness of the FETi-flexor connection when the tibia is fully flexed, and thus to increase its adaptive advantage during the co-contraction preceding a jump or kick, and to reduce the effectiveness of the connection when the tibia is partially or fully extended, and thus to reduce its potentially maladaptive consequences during voluntary extension movements such as thrusting.

A miniaturized cuff electrode for electrical stimulation of peripheral nerves in the freely moving rat.

A bipolar cuff electrode for electrical stimulation of small diameter peripheral nerves is described. The cuff is made of a highly flexible rubber-impression material, and the electrode assembly is suited for chronic implantation. Its manual construction is easy and reliable, utilizing only simple tools. The cuff completely envelopes nerves of varying diameter and requires a minimal amount of manipulations of the nerve, thereby reducing the chance of surgical trauma. The snug envelope prevents the nerve from drying, and minimizes shunting between the two leads by extracellular fluids. Small outer dimensions were achieved: 1.4 x 1.1 x 2.3 mm (width x height x length) when used with nerves of 1 mm diameter, which minimizes pressure and damage to surrounding tissues. Morphometric analysis of nerves enclosed in cuffs for 28-30 h revealed a small decrease in the number of large-diameter fibers. Stimulation thresholds remained, however, constant throughout the experiments.

A slim needle-shaped multiwire microelectrode for intracerebral recording.

The construction of a needle-shaped multiwire microelectrode is described. It can be made with simple mechanical tools. The presented electrode assembly consists of 12 insulated nichrome wires (core diameter 25 microns) which are embedded in epoxylite resin. The straight-cut wire tips are aligned lengthwise and have a relative spacing of 150 microns. Outer dimensions vary from 100 x 180 microns at the level of the 1st electrode channel, to 100 x 100 microns at the level of the 12th channel at the tip. The configuration of this electrode was determined by its application: the laminar analysis of evoked potentials in the cortex of the rat. However, the number of channels, the diameter of the (nichrome) wire which determines the surface area of these channels, and the channel spacing can be easily adjusted during construction to meet other experimental requirements, such as the recording of single-unit activity. The electrode which is composed of biocompatible materials is suited for the study of field potentials and multiple-unit activity, in both acute and chronic experiments, and can be used repeatedly. To demonstrate the performance of the electrode assembly, a depth profile of field potentials is presented, accompanied by the corresponding current source density distribution. The potentials were recorded in the somatosensory cortex of the rat following stimulation of the median nerve under ketamine anesthesia.