Learning alters theta amplitude, theta-gamma coupling and neuronal synchronization in inferotemporal cortex.

BACKGROUND: How oscillatory brain rhythms alone, or in combination, influence cortical information processing to support learning has yet to be fully established. Local field potential and multi-unit neuronal activity recordings were made from 64-electrode arrays in the inferotemporal cortex of conscious sheep during and after visual discrimination learning of face or object pairs. A neural network model has been developed to simulate and aid functional interpretation of learning-evoked changes. RESULTS: Following learning the amplitude of theta (4-8 Hz), but not gamma (30-70 Hz) oscillations was increased, as was the ratio of theta to gamma. Over 75% of electrodes showed significant coupling between theta phase and gamma amplitude (theta-nested gamma). The strength of this coupling was also increased following learning and this was not simply a consequence of increased theta amplitude. Actual discrimination performance was significantly correlated with theta and theta-gamma coupling changes. Neuronal activity was phase-locked with theta but learning had no effect on firing rates or the magnitude or latencies of visual evoked potentials during stimuli. The neural network model developed showed that a combination of fast and slow inhibitory interneurons could generate theta-nested gamma. By increasing N-methyl-D-aspartate receptor sensitivity in the model similar changes were produced as in inferotemporal cortex after learning. The model showed that these changes could potentiate the firing of downstream neurons by a temporal desynchronization of excitatory neuron output without increasing the firing frequencies of the latter. This desynchronization effect was confirmed in IT neuronal activity following learning and its magnitude was correlated with discrimination performance. CONCLUSIONS: Face discrimination learning produces significant increases in both theta amplitude and the strength of theta-gamma coupling in the inferotemporal cortex which are correlated with behavioral performance. A network model which can reproduce these changes suggests that a key function of such learning-evoked alterations in theta and theta-nested gamma activity may be increased temporal desynchronization in neuronal firing leading to optimal timing of inputs to downstream neural networks potentiating their responses. In this way learning can produce potentiation in neural networks simply through altering the temporal pattern of their inputs.

Behavioural and neurophysiological evidence for face identity and face emotion processing in animals.

Visual cues from faces provide important social information relating to individual identity, sexual attraction and emotional state. Behavioural and neurophysiological studies on both monkeys and sheep have shown that specialized skills and neural systems for processing these complex cues to guide behaviour have evolved in a number of mammals and are not present exclusively in humans. Indeed, there are remarkable similarities in the ways that faces are processed by the brain in humans and other mammalian species. While human studies with brain imaging and gross neurophysiological recording approaches have revealed global aspects of the face-processing network, they cannot investigate how information is encoded by specific neural networks. Single neuron electrophysiological recording approaches in both monkeys and sheep have, however, provided some insights into the neural encoding principles involved and, particularly, the presence of a remarkable degree of high-level encoding even at the level of a specific face. Recent developments that allow simultaneous recordings to be made from many hundreds of individual neurons are also beginning to reveal evidence for global aspects of a population-based code. This review will summarize what we have learned so far from these animal-based studies about the way the mammalian brain processes the faces and the emotions they can communicate, as well as associated capacities such as how identity and emotion cues are dissociated and how face imagery might be generated. It will also try to highlight what questions and advances in knowledge still challenge us in order to provide a complete understanding of just how brain networks perform this complex and important social recognition task.

The locust tegula: kinematic parameters and activity pattern during the wing stroke.

The tegula is a complex, knob-shaped sense organ associated with the base of the locust wing. Despite a detailed knowledge of its role in flight motor control, little is known about the relationship between the stroke parameters of the wing, movement of the tegula organ and the pattern of tegula activity. In this study, therefore, the kinematic parameters of the fore- and hindwings were investigated with respect to the tegula activity pattern during tethered flight. The following results were obtained. (i) The tegula moves through a complex three-dimensional trajectory during the wing stroke, involving inclination and rotation about its longitudinal axis. (ii) The kinematic parameters of tegula movement are phase-locked to the wing stroke and vary in conjunction with wing stroke parameters such as amplitude and cycle period. (iii) In accordance with these phase-locked kinematics, both the onset of tegula activity with respect to the downstroke (latency) and the discharge of the organ (burst duration and amplitude) vary in conjunction with downstroke movement and cycle period, resulting in an (almost) constant phase of tegula activation during the stroke cycle. (iv) The pattern of tegula activity during flight is largely independent of stroke amplitude. (v) The latency, burst duration and amplitude of tegula activity are strongly related to the angular velocity of the wing during the downstroke, with latency reaching a steady minimum value at higher angular velocities. The data suggest that the tegula encodes the timing and velocity of the downstroke and that it may be involved in the control of the stroke's angular velocity.

Alpha-adrenoreceptor activation modulates swimming via glycinergic and GABAergic inhibitory pathways in Xenopus laevis tadpoles.

This study focuses upon the network pathways underlying the adrenoreceptor-mediated modulation of fictive swimming in the immobilized Xenopus laevis tadpole. As shown recently, noradrenaline (NA) increases cycle periods while simultaneously reducing the rostrocaudal delay in head-to-tail firing and the duration of swimming episodes. Furthermore, both swimming frequency and duration are reduced by selective pharmacological activation of alpha1- and/or alpha2-adrenoreceptors, while alpha1-receptor activation also reduces rostrocaudal delays. We show that NA could still modulate aspects of swimming after blocking either glycine or GABA(A) receptors with strychnine and bicuculline, respectively. Furthermore, after prior application of NA, strychnine could counteract noradrenergic effects on cycle periods and rostrocaudal delays, while bicuculline could counteract effects on cycle periods, suggesting that these two fast inhibitory pathways are both involved in the NA modulation of swimming. In addition, blocking glycine receptors reduced the effects of alpha1-receptors on cycle periods and delays, while blocking GABA(A) receptors had no effect. Blocking either glycine or GABA(A) receptors, however, lessened the reduction in swimming frequency by alpha2-receptors. In addition, pre-application of bicuculline prevented a reduction in episode durations by NA, alpha1- and alpha2-receptors. Our findings suggest that the noradrenergic modulation of Xenopus swimming is mediated via alpha-adrenoreceptors interacting with both glycinergic and GABAergic inhibitory pathways. Both alpha1- and alpha2-receptor activation influences the GABAergic pathway controlling the duration of swimming episodes and is involved in the glycinergic modulation of the swimming rhythm and its longitudinal co-ordination, with alpha2-receptors additionally affecting swimming frequency through GABAergic pathways.

Fast inhibitory synapses: targets for neuromodulation and development of vertebrate motor behaviour.

Locomotor networks must possess the inherent flexibility to adapt their output. In this review we discuss evidence from a simple vertebrate locomotor network that suggests fast inhibitory synapses are important targets for the forms of neuromodulation that afford this flexibility. Two important inhibitory transmitters, glycine and GABA, are present in the CNS of Xenopus tadpoles, where they each play distinct roles in the control of swimming. Glycine, but not GABA, contributes to the inhibitory mid-cycle component of each swim-cycle, the strength of which determines the frequency of swimming. Meanwhile, GABA release onto the swim network prematurely terminates swimming episodes. Hence, glycine controls how fast, whilst GABA controls how far the tadpole swims. Our work has focused on how the amines serotonin (5-HT) and noradrenaline (NA), and more recently the gas nitric oxide (NO), selectively target glycine and GABA release in the spinal cord to modulate swimming. In particular, we have identified three brainstem populations of nitrergic neurons, which suggests that nitric oxide may co-localise with 5-HT, NA and GABA. Here we review this work and suggest a hierarchy of brainstem modulatory systems, with NO acting as a metamodulator.