Mathew E. Diamond

Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study

The intensity and spatial distribution of functional activation in the left precentral and postcentral gyri during actual motor performance (MP) and mental representation [motor imagery (MI)] of self-paced finger-to-thumb opposition movements of the dominant hand were investigated in fourteen right-handed volunteers by functional magnetic resonance imaging (fMRI) techniques. Significant increases in mean normalized fMRI signal intensities over values obtained during the control (visual imagery) tasks were found in a region including the anterior bank and crown of the central sulcus, the presumed site of the primary motor cortex, during both MP (mean percentage increase, 2.1%) and MI (0.8%). In the anterior portion of the precentral gyrus and the postcentral gyrus, mean functional activity levels were also increased during both conditions (MP, 1.7 and 1.2%; MI, 0.6 and 0.4%, respectively). To locate activated foci during MI, MP, or both conditions, the time course of the signal intensities of pixels lying in the precentral or postcentral gyrus was plotted against single-step or double-step waveforms, where the steps of the waveform corresponded to different tasks. Pixels significantly (r > 0.7) activated during both MP and MI were identified in each region in the majority of subjects; percentage increases in signal intensity during MI were on average 30% as great as increases during MP. The pixels activated during both MP and MI appear to represent a large fraction of the whole population activated during MP. These results support the hypothesis that MI and MP involve overlapping neural networks in perirolandic cortical areas.

The Role of Spike Timing in the Coding of Stimulus Location in Rat Somatosensory Cortex

Although the timing of single spikes is known to code for time-varying features of a sensory stimulus, it remains unclear whether time is also exploited in the neuronal coding of the spatial structure of the environment, where nontemporal stimulus features are fundamental. This report demonstrates that, in the whisker representation of rat cortex, precise spike timing of single neurons increases the information transmitted about stimulus location by 44%, compared to that transmitted only by the total number of spikes. Crucial to this code is the timing of the first spike after whisker movement. Complex, single neuron spike patterns play a smaller, synergistic role. Timing permits very few spikes to transmit high quantities of information about a behaviorally significant, spatial stimulus.

Active sensation: insights from the rodent vibrissa sensorimotor system

Rats sweep their vibrissae through space to locate objects in their immediate environment. In essence, their view of the proximal world is generated through pliable hairs that tap and palpate objects. The texture and shape of those objects must be discerned for the rat to assess the value of the object. Furthermore, the location of those objects must be specified with reference to the position of the rats head for the rat to plan its movements. Recent in vivo and in vitro electrophysiological measurements provide insight into the algorithms and mechanisms that underlie these behavioral-based computations.

An innocuous bias in whisker use in adult rats modifies receptive fields of barrel cortex neurons

The effect of innocuously biasing the flow of sensory activity from the whiskers for periods of 3–30 d in awake, behaving adult rats on the receptive field organization of rat SI barrel cortex neurons was studied. One pair of adjacent whiskers, D2 and either D1 or D3, remained intact unilaterally (whisker pairing), all others being trimmed throughout the period of altered sensation. Receptive fields of single cells in the contralateral D2 barrel were analyzed under urethane anesthesia by peristimulus time histogram (PSTH) and latency histogram analysis after 3, 7–10, and 30 d of pairing and compared with controls, testing all whiskers cut to the same length. Response magnitudes to surround receptive field in-row whiskers D1 and D3 were not significantly different for control animals. The same was found for surround in-arc whiskers C2 and E2. However, after 3 d of whisker pairing a profound bias occurred in response to the paired D-row surround whisker relative to the opposite trimmed surround D-row whisker and to the C2 and E2 whiskers. This bias increased with the duration of pairing, regardless of which surround whisker (D1 or D3) was paired with D2. For all three periods of pairing the mean response to the paired surround whisker was increased relative to controls, but peaked at 7–10 d. Response to the principal center-receptive (D2) whisker was increased for the 3 and 7–10 d groups and then decreased at 30 d. Responses to trimmed arc surround whiskers (C2 and E2) were decreased in proportion to the duration of changed experience. Analysis of PSTH data showed that earliest discharges (5–10 msec poststimulus) to the D2 whisker increased progressively in magnitude with duration of pairing. For the paired surround whisker similar early discharges newly appeared after 30 d of pairing. At 3 and 7–10 d of pairing, increases in response to paired whiskers and decreases to cut surround whiskers were confined to late portions of the PSTH (10–100 msec poststimulus). Changes at 3–10 d can be attributed to alterations in intracortical synaptic relay between barrels. Longer-term changes in response to both paired whisker inputs (30 d) largely appear to reflect increases in thalamocortical synaptic efficacy. Our findings suggest that novel innocuous somatosensory experiences produce changes in the receptive field configuration of cortical cells that are consistent with Hebbian theories of experience-dependent potentiation and weakening of synaptic efficacy within SI neocortical circuitry, for correlated and uncorrelated sensory inputs, respectively.

Neuronal Activity in Rat Barrel Cortex Underlying Texture Discrimination

Rats and mice palpate objects with their whiskers to generate tactile sensations. This form of active sensing endows the animals with the capacity for fast and accurate texture discrimination. The present work is aimed at understanding the nature of the underlying cortical signals. We recorded neuronal activity from barrel cortex while rats used their whiskers to discriminate between rough and smooth textures. On whisker contact with either texture, firing rate increased by a factor of two to ten. Average firing rate was significantly higher for rough than for smooth textures, and we therefore propose firing rate as the fundamental coding mechanism. The rat, however, cannot take an average across trials, but must make an immediate decision using the signals generated on each trial. To estimate single-trial signals, we calculated the mutual information between stimulus and firing rate in the time window leading to the rats observed choice. Activity during the last 75 ms before choice transmitted the most informative signal; in this window, neuronal clusters carried, on average, 0.03 bits of information about the stimulus on trials in which the rats behavioral response was correct. To understand how cortical activity guides behavior, we examined responses in incorrect trials and found that, in contrast to correct trials, neuronal firing rate was higher for smooth than for rough textures. Analysis of high-speed films suggested that the inappropriate signal on incorrect trials was due, at least in part, to nonoptimal whisker contact. In conclusion, these data suggest that barrel cortex firing rate on each trial leads directly to the animals judgment of texture.

Whisker Vibration Information Carried by Rat Barrel Cortex Neurons

Rats can make extremely fine texture discriminations by “whisking” their vibrissa across the surface of an object. We have investigated one hypothesis for the neuronal basis of texture representation by measuring how clusters of neurons in the barrel cortex of anesthetized rats encode the kinetic features of sinusoidal whisker vibrations. Mutual information analyses of spike counts led to a number of findings. Information about vibration kinetics became available as early as 6 msec after stimulus onset and reached a peak at ∼20-30 msec. Vibration speed, proportional to the product of vibration amplitude (A) and frequency (f), was the kinetic property most reliably reported by cortical neurons. Indeed, by measuring information when the complete stimulus set was collapsed into feature-defined groups, we found that neurons reduced the dimensionality of the stimulus from two features (A, f) to a single feature, the product Af. Moreover, because different neurons encode stimuli in the same manner, information loss was negligible even when the activity of separate neuronal clusters was pooled. This suggests a decoding scheme whereby target neurons could capture all available information simply by summating the signals from separate barrel cortex neurons. These results indicate that neuronal population activity provides sufficient information to allow nearly perfect discrimination of two vibrations, based on their deflection speeds, within a time scale comparable with that of a single whisking motion across a surface.

Deciphering the Spike Train of a Sensory Neuron: Counts and Temporal Patterns in the Rat Whisker Pathway

Rats achieve remarkable texture discriminations by sweeping their facial whiskers along surfaces. This work explores how neurons at two levels of the sensory pathway, trigeminal ganglion and barrel cortex, carry information about such stimuli. We identified two biologically plausible coding mechanisms, spike counts and patterns, and used “mutual information” to quantify how reliably neurons in anesthetized rats reported texture when “decoded” according to these candidate mechanisms. For discriminations between surfaces of different coarseness, spike counts could be decoded reliably and rapidly (within 30 ms after stimulus onset in cortex). Information increased as responses were considered as spike patterns with progressively finer temporal precision. At highest temporal resolution (spike sequences across six bins of 4 ms), the quantity of “information” in patterns rose 150% for ganglion neurons and 110% for cortical neurons above that in spike counts. In some cases, patterns permitted discriminations not supported by spike counts alone.

Encoding of whisker vibration by rat barrel cortex neurons: implications for texture discrimination.

Rats, using their whiskers, have excellent capabilities in texture discrimination. What is the representation of texture in rat somatosensory cortex? We hypothesize that as rats “whisk” over a surface, the spatial frequency of a grooved or pebbled texture is converted to a temporal frequency of whisker vibration. Surface features such as groove depth or grain size modulate the amplitude of this vibration. Validation of the hypothesis depends on showing that vibration parameters have distinct neuronal representations in cortex. To test this, we delivered sinusoidal vibrations to the whisker shaft and analyzed cortical neuronal activity. Seven amplitudes and seven frequencies were combined to construct 49 stimuli while recording activity through a 10 × 10 microelectrode array inserted into the middle layers of barrel cortex. We find that cortical neurons do not explicitly encode vibration frequency (f) or amplitude (A) by any coding measure (average spike counts over different time windows, spike timing patterns in the peristimulus time histograms or in autocorrelograms). Instead, neurons explicitly encode the product of frequency and amplitude, which is proportional to the mean speed of the vibration. The quantity Af is an invariant because neuronal response encodes this feature independently of the values of the individual terms A and f. This was true across a wide time scale of firing rate measurements, from 5 to 500 msec. We conclude that vibration kinetics are rapidly and reliably encoded in the firing rate of cortical ensembles. Therefore, the cortical representation of vibration speed could underlie texture discrimination.

Somatosensory cortical neuronal population activity across states of anaesthesia

Experiments were carried out to learn about changes in sensory cortical processing associated with different levels of anaesthesia. Traditionally this question has been addressed by studying single neurons. Because state changes are likely to influence the relationships between neurons, the present experiments were undertaken to investigate the spatial and temporal firing patterns distributed across cortex. Using 5 × 5 or 10 × 10 microelectrode arrays, spontaneous and stimulus‐evoked activity of multineuron clusters was recorded from rat somatosensory ‘barrel’ cortex (the whisker representation) during a light surgical stage of urethane anaesthesia, and after two supplemental doses of urethane which led to intermediate and deep levels of anaesthesia. At all depths of anaesthesia, spontaneously occurring action potentials at a single electrode tended to be clustered into ‘bursts.’ With increasing anaesthetic depth, bursts became more prominent and rhythmic, and increasingly synchronized between cortical barrel‐columns. Burst frequency decreased and fewer spikes occurred outside bursts, leading to a decrease in the overall spontaneous firing rate. The cortical territory engaged by individual whiskers contracted with increasing depth of anaesthesia, leading to the spatial segregation of whisker representations. At all stages of anaesthesia, whisker stimulation produced the maximal cortical response when delivered close to burst onset. These observations show that ongoing spontaneous activity modulates sensory response properties and makes peripheral tactile information accessible to a cortical territory whose size is determined by the phase of burst cycle. The possible significance of the cyclic cortical responsiveness encountered during urethane anaesthesia to cortical processing in awake rats is considered.

Active touch sensing

Active sensing systems are purposive and information-seeking sensory systems. Active sensing usually entails sensor movement, but more fundamentally, it involves control of the sensor apparatus, in whatever manner best suits the task, so as to maximize information gain. In animals, active sensing is perhaps most evident in the modality of touch. In this theme issue, we look at active touch across a broad range of species from insects, terrestrial and marine mammals, through to humans. In addition to analysing natural touch, we also consider how engineering is beginning to exploit physical analogues of these biological systems so as to endow robots with rich tactile sensing capabilities. The different contributions show not only the varieties of active touch—antennae, whiskers and fingertips—but also their commonalities. They explore how active touch sensing has evolved in different animal lineages, how it serves to provide rapid and reliable cues for controlling ongoing behaviour, and even how it can disintegrate when our brains begin to fail. They demonstrate that research on active touch offers a means both to understand this essential and primary sensory modality, and to investigate how animals, including man, combine movement with sensing so as to make sense of, and act effectively in, the world.