Neural Population Structures and Consequences for Neural Coding

Researchers studying neural coding have speculated that populations of neurons would more effectively represent the stimulus if the neurons "cooperated:" by interacting through lateral connections, the neurons would process and represent information better than if they functioned independently. We apply our new theory of information processing to determine the fidelity limits of simple population structures to encode stimulus features. We focus on noncooperative populations, which have no lateral connections. We show that they always exhibit positively correlated responses and that as population size increases, they perfectly represent the information conveyed by their inputs regardless of the individual neuron's coding scheme. Cooperative populations, which do have lateral connections, can, depending on the nature of the connections, perform better or worse than their noncooperative counterparts. We further show that common notions of synergy fail to capture the level of cooperation and to reflect the information processing properties of populations.     

Great apes track hidden objects after changes in the objects' position and in subject's orientation

Eight chimpanzees (Pan troglodytes), five bonobos (Pan paniscus), five gorillas (Gorilla gorilla), and seven orangutans (Pongo pygmaeus) were presented with two invisible object displacement tasks. In full view of the subject, a food item was hidden under one of three opaque cups resting on a platform and, after an experimental manipulation, the subject was allowed to select one of the cups. In the rotation task, the platform was rotated 180° while the subject remained stationary. In the translocation task, the platform remained stationary while the subject walked to the opposite side from where she saw the reward being hidden. The final position of the food relative to the subject was equivalent in both tasks. Single displacement trials consisted of only one manipulation, either a rotation or a translocation, whereas double displacement trials consisted of both a rotation and a translocation. We also included no displacement trials in which no displacements took place. No displacement trials were easier than single displacements which, in turn, were easier than double displacements. Unlike earlier studies with children, there was no difference in performance between rotation and translocation displacements. Overall, apes performed above chance in all conditions, but chimpanzees outperformed the other species. This study reinforces the notion that the great apes use an allocentric spatial coding. Am. J. Primatol. 72:349–359, 2010. © 2010 Wiley‐Liss, Inc.     

The state of gustatory neural coding

Debates on gustatory neural coding have been dominated by asmall number of fundamental issues since the inception of thefield in 1941. Three of these are discussed in this review:(1) are there basic tastes? (2) are there gustatory neuron types?(3) is the code for a taste read simultaneously across all participatingneurons (across-fiber patterning), or is it confined to a selectivechannel composed of cells of one type (labeled-line or channeling)?No conclusions are drawn regarding (1), primarily because auniversal definition of ‘basic tastes’ is lacking.It is concluded that gustatory neuron types are likely to existafter reviewing the issue from multiple perspectives and discoveringrecurring indications of neuron types from several. A firm conclusion,however, also awaits a widely accepted definition of what constitutesa neuron type. Issue (3) cannot yet be resolved for lack ofdefinitive data, specifically whether the discharges of inhibited,unresponsive, or weakly responsive cells add to (signal) ordetract from (noise) the neural code for a tastant.     

Optimal Stimulus Coding by Neural Populations Using Rate Codes

We create a framework based on Fisher information for determining the most effective population coding scheme for representing a continuous-valued stimulus attribute over its entire range. Using this scheme, we derive optimal single- and multi-neuron rate codes for homogeneous populations using several statistical models frequently used to describe neural data. We show that each neuron's discharge rate should increase quadratically with the stimulus and that statistically independent neural outputs provides optimal coding. Only cooperative populations can achieve this condition in an informationally effective way.     

综述: 初级视皮层的亮度信息加工

亮度(luminance)是最基本的视觉信息.与其他视觉特征相比,由于视神经元对亮度刺激的反应较弱,并且许多神经元对均匀亮度无反应,对亮度信息编码的神经机制知之甚少.初级视皮层部分神经元对亮度的反应要慢于对比度反应,被认为是由边界对比度诱导的亮度知觉(brightness)的神经基础.我们的研究表明,初级视皮层许多神经元的亮度反应要快于对比度反应,并且这些神经元偏好低的空间频率、高的时间频率和高的运动速度,提示皮层下具有低空间频率和高运动速度通路的信息输入对产生初级视皮层神经元的亮度反应有贡献.已经知道初级视皮层神经元对空间频率反应的时间过程是从低空间频率到高空间频率,我们发现的早期亮度反应是对极低空间频率的反应,与这一时间过程是一致的,是这一从粗到细的视觉信息加工过程的第一步,揭示了处理最早的粗的视觉信息的神经基础.另外,初级视皮层含有偏好亮度下降和高运动速度的神经元,这群神经元的活动有助于在光照差的环境中检测高速运动的低亮度物体.     

Information-Theoretic Analysis of Neural Coding

We describe an approach to analyzing single- and multiunit (ensemble) discharge patterns based on information-theoretic distance measures and on empirical theories derived from work in universal signal processing. In this approach, we quantify the difference between response patterns, whether time-varying or not, using information-theoretic distance measures. We apply these techniques to single- and multiple-unit processing of sound amplitude and sound location. These examples illustrate that neurons can simultaneously represent at least two kinds of information with different levels of fidelity. The fidelity can persist through a transient and a subsequent steady-state response, indicating that it is possible for an evolving neural code to represent information with constant fidelity.     

The rate of information transfer of naturalistic stimulation by graded potentials

We present a method to measure the rate of information transfer for any continuous signals of finite duration without assumptions. After testing the method with simulated responses, we measure the encoding performance of Calliphora photoreceptors. We find that especially for naturalistic stimulation the responses are nonlinear and noise is nonadditive, and show that adaptation mechanisms affect signal and noise differentially depending on the time scale, structure, and speed of the stimulus. Different signaling strategies for short- and long-term and dim and bright light are found for this graded system when stimulated with naturalistic light changes.     

Searching for Optimal Sensory Signals: Iterative Stimulus Reconstruction in Closed-Loop Experiments

Shaped by evolutionary processes, sensory systems often represent behaviorally relevant stimuli with higher fidelity than other stimuli. The stimulus dependence of neural reliability could therefore provide an important clue in a search for relevant sensory signals. We explore this relation and introduce a novel iterative algorithm that allows one to find stimuli that are reliably represented by the sensory system under study. To assess the quality of a neural representation, we use stimulus reconstruction methods. The algorithm starts with the presentation of an initial stimulus (e.g. white noise). The evoked spike train is recorded and used to reconstruct the stimulus online. Within a closed-loop setup, this reconstruction is then played back to the sensory system. Iterating this procedure, the newly generated stimuli can be better and better reconstructed. We demonstrate the feasibility of this method by applying it to auditory receptor neurons in locusts. Our data show that the optimal stimuli often exhibit pronounced sub-threshold periods that are interrupted by short, yet intense pulses. Similar results are obtained for simple model neurons and suggest that these stimuli are encoded with high reliability by a large class of neurons.     

大鼠损伤神经的三种诱发簇放电节律

实验运用单纤维记录技术,观察了损伤神经起步点自发放电在改变[Ca^2 ]。和veratridine作用下放电节律的变化。结果表明：在每一标本上,记录到的相同背景的自发放电在低与高Ca^2 浓度和veratridine的作用下,转化为三种不同类型的簇放电。结果提示,神经元放电的节律形式与刺激的性质相关,不同的节律形式可能携带着不同的神经信息。     

Noise,not stimulus entropy,determines neural information rate

In the quest for deciphering the neural code, theoretical advances were made which allow for the determination of the information rate inherent in the spike trains of nerve cells. However, up to now, the dependence of the information rate on stimulus parameters has not been studied in any neuron in a systematic way. Here, I investigate the information carried by the spike trains of H1, a motion-sensitive visual interneuron of the blowfly (Calliphora vicina) using a moving grating as a stimulus. Stimulus parameters fall in two classes: those that have only a minor effect on the information rate like increasing the frequency bandwidth or the maximum amplitude of the stimulus velocity, and those which dramatically affect the neural information rate, like varying the spatial size or the contrast of the visual pattern being moved. It appears that, for a broad range of complex stimuli, the neuron covers the stimulus with its whole response repertoire regardless of the stimulus entropy, with the information rate being limited by the noise of the stimulus and the neural hardware.     

Pulse trains to percepts: the challenge of creating a perceptually intelligible world with sight recovery technologies

An extraordinary variety of sight recovery therapies are either about to begin clinical trials, have begun clinical trials, or are currently being implanted in patients. However, as yet we have little insight into the perceptual experience likely to be produced by these implants. This review focuses on methodologies, such as optogenetics, small molecule photoswitches and electrical prostheses, which use artificial stimulation of the retina to elicit percepts. For each of these technologies, the interplay between the stimulating technology and the underlying neurophysiology is likely to result in distortions of the perceptual experience. Here, we describe some of these potential distortions and discuss how they might be minimized either through changes in the encoding model or through cortical plasticity.     

Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 degrees C

Besides the physical limits imposed on photon absorption, the coprocessing of visual information by the phototransduction cascade and photoreceptor membrane determines the fidelity of photoreceptor signaling. We investigated the response dynamics and signaling efficiency of Drosophila photoreceptors to natural-like fluctuating light contrast stimulation and intracellular current injection when the cells were adapted over a 4-log unit light intensity range at 25 degrees C. This dual stimulation allowed us to characterize how an increase in the mean light intensity causes the phototransduction cascade and photoreceptor membrane to produce larger, faster and increasingly accurate voltage responses to a given contrast. Using signal and noise analysis, this appears to be associated with an increased summation of smaller and faster elementary responses (i.e., bumps), whose latency distribution stays relatively unchanged at different mean light intensity levels. As the phototransduction cascade increases, the size and speed of the signals (light current) at higher adapting backgrounds and, in conjunction with the photoreceptor membrane, reduces the light-induced voltage noise, and the photoreceptor signal-to-noise ratio improves and extends to a higher bandwidth. Because the voltage responses to light contrasts are much slower than those evoked by current injection, the photoreceptor membrane does not limit the speed of the phototransduction cascade, but it does filter the associated high frequency noise. The photoreceptor information capacity increases with light adaptation and starts to saturate at approximately 200 bits/s as the speed of the chemical reactions inside a fixed number of transduction units, possibly microvilli, is approaching its maximum.     

Light adaptation in Drosophila photoreceptors: II. Rising temperature increases the bandwidth of reliable signaling

It is known that an increase in both the mean light intensity and temperature can speed up photoreceptor signals, but it is not known whether a simultaneous increase of these physical factors enhances information capacity or leads to coding errors. We studied the voltage responses of light-adapted Drosophila photoreceptors in vivo from 15 to 30 degrees C, and found that an increase in temperature accelerated both the phototransduction cascade and photoreceptor membrane dynamics, broadening the bandwidth of reliable signaling with an effective Q(10) for information capacity of 6.5. The increased fidelity and reliability of the voltage responses was a result of four factors: (1) an increased rate of elementary response, i.e., quantum bump production; (2) a temperature-dependent acceleration of the early phototransduction reactions causing a quicker and narrower dispersion of bump latencies; (3) a relatively temperature-insensitive light-adapted bump waveform; and (4) a decrease in the time constant of the light-adapted photoreceptor membrane, whose filtering matched the dynamic properties of the phototransduction noise. Because faster neural processing allows faster behavioral responses, this improved performance of Drosophila photoreceptors suggests that a suitably high body temperature offers significant advantages in visual performance.     

Temporal encoding in nervous systems: A rigorous definition

We propose a rigorous definition for the termtemporal encoding as it is applied to schemes for the representation of information withinpatterns of neuronal action potentials, and distinguish temporal encoding schemes from those based on window-averagedmean rate encoding. The definition relies on the identification of anencoding time window, defined as the duration of a neuron's spike train assumed to correspond to a single symbol in the neural code. The duration of the encoding time window is dictated by the time scale of the information being encoded. We distinguish between the concepts of theencoding time window and theintegration time window, the latter of which is defined as the duration of a stimulus signal that affects the response of the neuron. We note that the duration of the encoding and integration windows might be significantly different. We also present objective, experimentally assessable criteria for identifying neurons and neuronal ensembles that utilize temporal encoding to any significant extent. The definitions and criteria are made rigorous within the contexts of several commonly used analytical approaches, including thestimulus reconstruction analysis technique. Several examples are presented to illustrate the distinctions between and relative capabilities of rate encoding and temporal encoding schemes. We also distinguish our usage oftemporal encoding from the termtemporal coding, which is commonly used in reference to the representation of information about thetiming of events by rate encoding schemes.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.