Encoding the expectation of a sensory stimulus

Most organisms possess an ability to differentiate unexpected or surprising sensory stimuli from those that are repeatedly encountered. How is this sensory computation performed? We examined this issue in the locust olfactory system. We found that odor-evoked responses in the antennal lobe (downstream to sensory neurons) systematically reduced upon repeated encounters of a temporally discontinuous stimulus. Rather than confounding information about stimulus identity and intensity, neural representations were optimized to encode equivalent stimulus-specific information with fewer spikes. Further, spontaneous activity of the antennal lobe network also changed systematically and became negatively correlated with the response elicited by the repetitive stimulus (i.e. ‘a negative image’). Notably, while response to the repetitive stimulus reduced, exposure to an unexpected/deviant cue generated undamped and even exaggerated spiking responses in several neurons. In sum, our results reveal how expectation regarding a stimulus is encoded in a neural circuit to allow response optimization and preferential filtering.

Intracellular calcium movements during relaxation and recovery of superfast muscle fibers of the toadfish swimbladder

The mating call of the Atlantic toadfish is generated by bursts of high-frequency twitches of the superfast twitch fibers that surround the swimbladder. At 16°C, a calling period can last several hours, with individual 80–100-Hz calls lasting ∼500 ms interleaved with silent periods (intercall intervals) lasting ∼10 s. To understand the intracellular movements of Ca2+ during the intercall intervals, superfast fibers were microinjected with fluo-4, a high-affinity fluorescent Ca2+ indicator, and stimulated by trains of 40 action potentials at 83 Hz, which mimics fiber activity during calling. The fluo-4 fluorescence signal was measured during and after the stimulus trains; the signal was also simulated with a kinetic model of the underlying myoplasmic Ca2+ movements, including the binding and transport of Ca2+ by the sarcoplasmic reticulum (SR) Ca2+ pumps. The estimated total amount of Ca2+ released from the SR during a first stimulus train is ∼6.5 mM (concentration referred to the myoplasmic water volume). At 40 ms after cessation of stimulation, the myoplasmic free Ca2+ concentration ([Ca2+]) is below the threshold for force generation (∼3 µM), yet the estimated concentration of released Ca2+ remaining in the myoplasm (Δ[CaM]) is large, ∼5 mM, with ∼80% bound to parvalbumin. At 10 s after stimulation, [Ca2+] is ∼90 nM (three times the assumed resting level) and Δ[CaM] is ∼1.3 mM, with 97% bound to parvalbumin. Ca2+ movements during the intercall interval thus appear to be strongly influenced by (a) the accumulation of Ca2+ on parvalbumin and (b) the slow rate of Ca2+ pumping that ensues when parvalbumin lowers [Ca2+] near the resting level. With repetitive stimulus trains initiated at 10-s intervals, Ca2+ release and pumping come quickly into balance as a result of the stability (negative feedback) supplied by the increased rate of Ca2+ pumping at higher [Ca2+].

Slow Recovery From Excitation of Thalamic Reticular Nucleus Neurons

Responses to repeated auditory stimuli were examined in 103 neurons in the auditory region of the thalamic reticular nucleus (TRN) and in 20 medial geniculate (MGB) neurons of anesthetized rats. A further six TRN neurons were recorded from awake rats. The TRN neurons showed strong responses to the first trial and weak responses to the subsequent trials of repeated auditory stimuli and electrical stimulation of the MGB and auditory cortex when the interstimulus interval (ISI) was short (<3 s). They responded to the second trial when the interstimulus interval was lengthened to ≥3 s. These responses contrasted to those of MGB neurons, which responded to repeated auditory stimuli of different ISIs. The TRN neurons showed a significant increase in the onset auditory response from 9.5 to 76.5 Hz when the ISI was increased from 200 ms to 10 s ( P < 0.001, ANOVA). The duration of the auditory-evoked oscillation was longer when the ISI was lengthened. The slow recovery of the TRN neurons after oscillation of burst firings to fast repetitive stimulus was a reflection of a different role than that of the thalamocortical relay neurons. Supposedly the TRN is involved in the process of attention such as attention shift; the slow recovery of TRN neurons probably limits the frequent change of the attention in a fast rhythm.

Stimulus-Evoked Modulation of Sensorimotor Pyramidal Neuron EPSPs

Sensory cortical neurons display substantial receptive field dynamics during and after persistent sensory drive. Because a cell's response properties are determined by the inputs it receives, receptive field dynamics are likely to involve changes in the relative efficacy of different inputs to the cell. To test this hypothesis, we have investigated if brief repetitive stimulus drive in vitro alters the efficacy of two types of corticocortical inputs to layer V pyramidal cells. Specifically, we have used whole cell recordings to measure the effect of repetitive electrical stimulation at the layer VI/white matter (WM) border on the synaptic response of layer V pyramidal cells to corticocortical input evoked by electrical stimulation of layer I or layer II/III and emulated by local application of glutamate. Repetitive stimulation (10 Hz for 3 s) at the layer VI/WM border transiently potentiated excitatory postsynaptic potentials (EPSPs) evoked by electrical stimulation of layer II/III by 97 ± 12% (mean ± SE). The recovery of EPSP amplitude to its preconditioning value was well-described by a single-term decaying exponential with a time constant of 7.2 s. The same layer VI/WM conditioning train that evoked layer II/III EPSP potentiation frequently caused an attenuation of layer I EPSPs. Similarly, subthreshold postsynaptic responses to local glutamate application in layers II/III and I were potentiated and attenuated, respectively, by the conditioning stimulus. Potentiation and attenuation could be evoked in the same cell by repositioning the glutamate puffer pipette in the appropriate layer. The conditioning stimulus that led to the transient modification of upper layer EPSP efficacy also evoked a slow depolarization in glial cells. The membrane potential of glial cells recovered with a time course similar to the dissipation of the potentiation effect, suggesting that stimulus-evoked changes in extracellular potassium (ECK) play a role in layer II/III EPSP potentiation. Consistent with this proposal, increasing the bath concentration of ECK caused a substantial increase of layer II/III EPSP amplitude. EPSP potentiation was sensitive to postsynaptic membrane potential and, more importantly, was significantly weaker for synaptic currents than for synaptic potentials, suggesting that it involves the recruitment of a postsynaptic voltage-dependent mechanism. Two observations suggest that layer II/III EPSP potentiation may involve the recruitment of postsynaptic sodium channels: EPSP potentiation was strongly reduced by intracellular application of N-(2,6-dimethyl-phenylcarbamoylmethyl) triethylammonium bromide (QX-314) and responses to local glutamate application were potentiated by high ECK in the presence of cadmium but not in the presence of tetrodotoxin. The results demonstrate a novel way in which brief periods of repetitive stimulus drive are accompanied by rapid, transient, and specific alterations in the functional connectivity and information processing characteristics of sensorimotor cortex.

Brain stem reticular influences on lumbar axial muscle activity. II. Temporal aspects

Epaxial muscle electromyographic (EMG) responses to electrical stimulation of the pontomedullary reticular formation were analyzed for temporal patterns in the urethan-anesthetized rat. Recordings were obtained from the transversospinalis, medial longissimus, and lateral longissimus groups of back muscles. In response to a series of repetitive stimulus trains, the latency of muscle activation decreased with successive trains. Typically a 10-fold decrease in latency required eight to nine stimulus trains (5 trains/s, 25 pulses/train) with currents of 25-30 microA. Individual pulses within long stimulus trains evoked muscle spike potentials at low probability but with short latencies (population range 4-7 ms). The results suggest that whereas influences on lumbar axial musculature from brain stem reticular formation were not powerful enough to evoke muscle spikes with single-pulse stimulation at currents applied in this study, they can yield short, relatively fixed EMG onset latencies in response to individual pulses within stimulus trains once a potentiation phenomenon has occurred.

The Laminar organization of optic nerve fibres in the tectum of goldfish

Potentials in the tectum of large (12─20 cm) goldfish, evoked by stimulation of the optic nerve, were recorded extracellularly with double-barrelled electrodes (d. c., saline and a. c., Woods metal─Pt). Four fibre groups (E, M 1 , M 2 , M 3 ) were recorded at latencies of approximately 2, 3, 5 and 8 ms after stimulation (conduction velocities of approximately 7, 5, 3 and 2 m/s). The same four groups were recorded from the optic nerve when the tectum was stimulated. The fastest fibre group (E) did not give rise to a postsynaptic wave. Fibre groups M 1 , M 2 and M 3 gave rise to postsynaptic potentials which, following computation of their second spatial derivatives with depth, were found to have current sinks at depths of approximately 100─50 μm, 150─200 μm and 250-350 μm respectively. Thus the fastest conducting retinotectal fibres make their synapses most superficially, the opposite of the arrangement in the frog tectum. These postsynaptic waves fatigued at repetitive stimulus rates of 20─50 per second, and in twin pulses at interstimulus intervals of 10─15 ms; and they were reversibly blocked by topical application of pentobarbitol. The fibre potentials, however, were virtually undecremented under these conditions. To compare these electrophysiological findings with the anatomy, the cobalt procedure was used to visualize the profiles of the optic fibres in the various tectal laminae. A thick dense projection filled the superficial grey and white (s. g. w.) layer, and there was a thin satellite band just superficial to it. In addition, there were two deeper bands of sparse innervation, in the middle of the central grey zone (c. g.) and in the deep white (d. w.) layer. These bands were associated with the field potential sinks through lesions made with recording electrodes. The two deep bands correspond to the M 3 fibre group. The dense s. g. w. innervation contains both the M 1 and M 2 fibre groups, the M 1 just superficial to the M 2 . The fastest fibre group, E, which had no postsynaptic wave associated with it, persisted at least six weeks after retinal removal, and probably represents efferent cells with fibres projecting back through the optic nerve to the retina. Filled cell profiles could not be positively identified with the cobalt technique, but could be seen with the HRP technique, when the optic afferents were first allowed to degenerate. The filled cells were the pyramidals of the s. g. w. layer.