Nikolaos C. Aggelopoulos

Cholinergic Control of Visual Categorization in Macaques

Acetylcholine (ACh) is a neurotransmitter acting via muscarinic and nicotinic receptors that is implicated in several cognitive functions and impairments, such as Alzheimer’s disease. It is believed to especially affect the acquisition of new information, which is particularly important when behavior needs to be adapted to new situations and to novel sensory events. Categorization, the process of assigning stimuli to a category, is a cognitive function that also involves information acquisition. The role of ACh on categorization has not been previously studied. We have examined the effects of scopolamine, an antagonist of muscarinic ACh receptors, on visual categorization in macaque monkeys using familiar and novel stimuli. When the peripheral effects of scopolamine on the parasympathetic nervous system were controlled for, categorization performance was disrupted following systemic injections of scopolamine. This impairment was observed only when the stimuli that needed to be categorized had not been seen before. In other words, the monkeys were not impaired by the central action of scopolamine in categorizing a set of familiar stimuli (stimuli which they had categorized successfully in previous sessions). Categorization performance also deteriorated as the stimulus became less salient by an increase in the level of visual noise. However, scopolamine did not cause additional performance disruptions for difficult categorization judgments at lower coherence levels. Scopolamine, therefore, specifically affects the assignment of new exemplars to established cognitive categories, presumably by impairing the processing of novel information. Since we did not find an effect of scopolamine in the categorization of familiar stimuli, scopolamine had no significant central action on other cognitive functions such as perception, attention, memory, or executive control within the context of our categorization task.

Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex

The sparseness of the encoding of stimuli by single neurons and by populations of neurons is fundamental to understanding the efficiency and capacity of representations in the brain, and was addressed as follows. The selectivity and sparseness of firing to visual stimuli of single neurons in the primate inferior temporal visual cortex were measured to a set of 20 visual stimuli including objects and faces in macaques performing a visual fixation task. Neurons were analysed with significantly different responses to the stimuli. The firing rate distribution of 36% of the neurons was exponential. Twenty-nine percent of the neurons had too few low rates to be fitted by an exponential distribution, and were fitted by a gamma distribution. Interestingly, the raw firing rate distribution taken across all neurons fitted an exponential distribution very closely. The sparseness as or selectivity of the representation of the set of 20 stimuli provided by each of these neurons (which takes a maximal value of 1.0) had an average across all neurons of 0.77, indicating a rather distributed representation. The sparseness of the representation of a given stimulus by the whole population of neurons, the population sparseness ap, also had an average value of 0.77. The similarity of the average single neuron selectivity as and population sparseness for any one stimulus taken at any one time ap shows that the representation is weakly ergodic. For this to occur, the different neurons must have uncorrelated tuning profiles to the set of stimuli.

Scene perception : inferior temporal cortex neurons encode the positions of different objects in the scene

Inferior temporal cortex (IT) neurons have reduced receptive field sizes in complex natural scenes. This facilitates the read‐out of information about individual objects from IT, but raises the question of whether more than the single object present at the fovea is represented by the firing of IT neurons, as would be important for whole scene perception in which several objects may be located without eye movements. Recordings from IT neurons with five simultaneously presented objects, each subtending 7°, with one object at the fovea and the other four centred 10° eccentrically in the parafovea, showed that although 38 IT neurons had their best response to an effective stimulus at the fovea, eight IT neurons had their best response to an object when it was located in one or more of the parafoveal positions. Moreover, of 54 neurons tested for asymmetric parafoveal receptive fields, 35 (65%) had significantly different responses for different parafoveal positions. The asymmetry was partly related to competition within the receptive fields, as only 21% of the neurons had significant asymmetries when tested with just one object present located at the same parafoveal positions. The findings thus show that some evidence is conveyed by a population of IT neurons about the relative positions of several simultaneously presented objects in a scene extending well into the parafovea during a single fixation, and this is likely to be important in whole scene perception with multiple objects, including specifying the relative positions of different objects in a scene.

The use of decoding to analyze the contribution to the information of the correlations between the firing of simultaneously recorded neurons

A new decoding method is described that enables the information that is encoded by simultaneously recorded neurons to be measured. The algorithm measures the information that is contained not only in the number of spikes from each neuron, but also in the cross-correlations between the neuronal firing including stimulus-dependent synchronization effects. The approach enables the effects of interactions between the ‘signal’ and ‘noise’ correlations to be identified and measured, as well as those from stimulus-dependent cross-correlations. The approach provides an estimate of the statistical significance of the stimulus-dependent synchronization information, as well as enabling its magnitude to be compared with the magnitude of the spike-count related information, and also whether these two contributions are additive or redundant. The algorithm operates even with limited numbers of trials. The algorithm is validated by simulation. It was then used to analyze neuronal data from the primate inferior temporal visual cortex. The main conclusions from experiments with two to four simultaneously recorded neurons were that almost all of the information was available in the spike counts of the neurons; that this Rate information included on average very little redundancy arising from stimulus-independent correlation effects; and that stimulus-dependent cross-correlation effects (i.e. stimulus-dependent synchronization) contribute very little to the encoding of information in the inferior temporal visual cortex about which object or face has been presented.

Non-uniform conduction time in the olivocerebellar pathway in the anaesthetized cat.

1. It has recently been demonstrated that conduction velocities of cerebellar climbing fibre afferents in the rat are tuned according to fibre length such that conduction time between their origin in the inferior olive and their target cortical Purkinje cells is constant. Here we have examined the situation in the cat, where individual climbing fibres are substantially longer. Complex spike responses of Purkinje cells located at various depths in the vermis (zones a and b) were evoked by electrical stimulation of olivocerebellar fibres close to their origin and were recorded either extra‐ or intracellularly. 2. The onset latencies of directly evoked complex spikes ranged from 2.6 to 6.9 ms. A consistent trend in each electrode penetration was that the complex spike latencies were longer for the superficially encountered cells (where olivocerebellar fibre length is greatest) and shorter for deeper cells (where olivocerebellar fibre length is shorter). 3. Linear regression analysis suggests that conduction time in olivocerebellar fibres in the cat is not fixed but varies linearly with conduction distance. Our findings would be consistent with a uniform conduction velocity in olivocerebellar fibres of about 6.6 m s‐1.

Information in the first spike, the order of spikes, and the number of spikes provided by neurons in the inferior temporal visual cortex.

Information theoretic analyses showed that for single inferior temporal neurons and neuronal populations, more information was encoded in 20 or more ms by all the spikes available than just by the first spike in the same time window about which of 20 objects or faces was shown. Further, the temporal order in which the first spike arrived from different simultaneously recorded neurons did not encode more information than was present in the first spike or the spike counts. Thus information transmission in the inferior temporal cortex by the number of spikes in even short time windows is fast, and provides more information than only the first spike, or the spike order from different neurons.

Segmental localisation of the relays mediating crossed inhibition of hindlimb motoneurones from group II afferents in the anaesthetized cat spinal cord

We have investigated the location of the spinal neurones mediating crossed inhibition from group II afferents. Short latency IPSPs are evoked in hindlimb extensor motoneurones by stimulation of specific contralateral limb nerves at stimuli sufficient to activate group II muscle afferents. Reversible or irreversible interruption of the dorsal columns in the fifth lumbar segment (L5) dramatically attenuated the crossed inhibition. It therefore appears that the central pathway mediating this crossed inhibition involves an interneuronal relay located in the L5 segment or further rostrally. As a consequence of this anatomy, the short central latency of the crossed IPSPs suggests that a single interneurone is involved.

Synaptogenesis in the dorsal lateral geniculate nucleus of the rat.

SummarySynapse formation and maturation were examined in the rat dorsal lateral geniculate nucleus (dLGN) from birth to adulthood. Examination of animals, whose ages were closely spaced in time, showed that the maturation of the synaptic organization of the nucleus takes place chiefly during the first 3 weeks of postnatal life. This period of maturation may be divided into 3 broad stages. During the first stage, which spans the first 4 days of life, there are only a few immature synapses scattered throughout the nucleus; occasionally aggregates of 3 or 4 synapses are encountered. Dendrodendritic synapses first appear at the end of this stage. The second stage, which lasts from the end of the first stage through day 8, is characterized by intensive synaptogenesis as well as extensive growth and degeneration. For the first time, large boutons resembling retinal terminals form multiple synaptic contacts with dendrites and dendritic protrusions; these synaptic arrangements are partially covered by glial processes.A feature characteristic of the developing dLGN during the first 2 postnatal weeks, and particularly during the second stage, is the presence of membrane specializations that resemble vacant postsynaptic densities. These specializations, which may be unapposed or opposite another neuronal process, decrease in frequency as the number of synapses increases. It is not known whether these densities are converted to synapses or whether they result from loss of presynaptic elements.The third stage in the process of synaptogenesis, which spans a period between days 10 and 20, is characterized by myelination and by the diminution of growth cones, degenerating profiles and vacant postsynaptic densities. There is also a very significant increase in the number and maturation of synapses including synaptic glomeruli. However, it is not until the end of this stage that synapses appear qualitatively indistinguishable from synaptic arrangements identified in adult animals.

Presynaptic control of transmission through group II muscle afferents in the midlumbar and sacral segments of the spinal cord is independent of corticospinal control.

Transmission of information from the terminals group II muscle afferents is subject to potent presynaptic modulation by both segmental group II and cutaneous afferents and by descending monoaminergic systems. Currently it is unknown whether descending corticospinal fibres affect this transmission. Here we have examined whether corticospinal tract activation modulates the size of monosynaptic focal synaptic potentials (FSPs) evoked by group II muscle afferents, and the excitability of intraspinal terminals of group II afferents, both of which are indices used to show presynaptic control. Conditioning stimulation of corticospinal pathways had no effects on the sizes of group II evoked FSPs in the midlumbar or sacral segments at either dorsal horn or intermediate zone locations. These stimuli also had no effect on the excitability of single group II afferent terminals in the dorsal horn of the midlumbar segments. As positive controls, we verified that the corticospinal conditioning stimuli used did effectively depress FSPs evoked from cutaneous afferents recorded at the same spinal locations as the group II field potentials in all experiments. Corticospinal tract conditioning stimuli did not consistently enhance or reduce the depression of group II FSPs that was evoked by stimulation of ipsilateral segmental group II or cutaneous afferents; in the large majority of cases there was no effect. The results reveal that the control of transmission of information from group II afferents in these regions of the spinal cord is independent of direct corticospinal control.

Activation of midlumbar neurones by afferents from anterior hindlimb muscles in the cat.

1. It has been suggested that a group of interneurones located in the midlumbar segments of the spinal cord might play a role in switching from the stance to swing phases of the step cycle during locomotion. We have further examined the input to these neurones from proprioceptive afferents to test whether the connections to these cells are consistent with this role. 2. Electrical stimulation of group I and group II afferents in branches of the femoral nerve which supply iliopsoas, the major hip flexor muscle, excited a large majority of intermediate zone midlumbar interneurones which receive input from quadriceps group II afferents. The central latencies and properties of the EPSPs indicate that both group I and group II afferents from iliopsoas make monosynaptic connections with many midlumbar interneurones. 3. Group II afferents from both the ankle flexor tibialis anterior and the digit dorsiflexor extensor digitorum longus excited midlumbar interneurones. Similarly, they were also excited by group II afferents from both of the two main anatomical divisions of the sartorius muscle. 4. The frequent and potent excitation of midlumbar neurones from group I and II afferents in iliopsoas suggests that they may be excited at the end of the stance phase of the step when these muscles are stretched. This possibility is discussed in relation to recent work on the functional control of the step cycle.