The psychophysical methods described in the previous section provide objective techniques for analyzing sensations evoked by particular stimuli. These quantitative measures have been combined with neurophysiological techniques to study the neural mechanisms that transform sensory signals into specific percepts.
This approach to the neural coding problem was pioneered by Vernon Mountcastle in the 1960s. He showed that neurophysiological recordings from individual sensory neurons in the peripheral and central nervous system provide a statistical description of the neural activity evoked by a physical stimulus. He then tested hypotheses to determine which quantitative aspects of the neural response might correspond to psychophysical measurements in sensory tasks, and just as important, which do not.
The study of neural coding of information is fundamental to understanding how the brain works. A neural code describes the relationship between the activity in a specified neural population and its functional consequences for the operations that follow. The sensory systems provide a useful avenue to the study of neural coding in the brain because both the input and output of these systems can be precisely defined and quantified. Experimenters can control the physical stimuli provided to sensory receptors and measure the resulting sensations evoked by them using a variety of psychophysical techniques. By recording neuronal activity at various stages of sensory processing, neuro scientists attempt to decipher the codes that convey information in peripheral nerves and in the brain, and analyze the transformation of signals along pathways in the cerebral cortex. Indeed, study of the details of neural coding may lead to insight into the coding principles that underlie cognition.
When analyzing sensory experience it is important to realize that our conscious sensations differ qualitatively from the physical properties of stimuli because, as Kant and the idealists predicted, the nervous system extracts only certain pieces of information from each stimulus while ignoring others. It then interprets this information within the constraints of the brain's intrinsic structure and previous experience. Thus we receive electromagnetic waves of different frequencies, but we see them as colors. We receive pressure waves from objects vibrating at different frequencies, but we hear sounds, words, and music. We encounter chemical compounds floating in the air or water, but we experience them as smells and tastes. Colors, tones, smells, and tastes are mental creations constructed by the brain out of sensory experience. They do not exist as such outside the brain.
The dominant research strategy in sensory neuro science is to follow the flow of sensory information from receptors toward the cognitive centers of the brain, attempting to understand the processing mechanisms that occur at each synaptic relay and how they shape our internal representation of the external world. The neural coding of sensory information is better understood at the early stages of processing than at later stages.
Sensory Receptors Are Responsive to a Single Type of Stimulus Energy
It is often said that the power of the brain lies in the millions of neurons processing information in parallel. That formulation, however, does not capture the essential difference between the brain and all the other organs of the body. The power of a kidney or a muscle lies in the parallel action of many cells, each doing the same thing; if we understand a muscle cell, we essentially understand how a whole muscle works. The power of the brain lies in the parallel action of millions of cells, each doing something different; to understand the brain we need to understand how its tasks are organized and how individual neurons carry out those tasks.
Functional differences between sensory systems arise from the different stimulus energies that drive them and the discrete pathways that comprise each system. Because of these characteristics each neuron performs a specific task, and the train of action potentials it produces has a specific functional significance for all postsynaptic neurons. This basic idea was expressed in the theory of specificity set forward by Charles Bell and Johannes Müller in the 19th century and remains one of the cornerstones of sensory neuroscience.
The richness of sensory experience begins with millions of highly specific sensory receptors. Each receptor responds to a specific kind of energy at specific locations on the body and sometimes only to energy with a particular temporal or spatial pattern. The receptor transforms the stimulus energy into electrical energy, thus establishing a common signaling mechanism in all sensory systems. The amplitude and duration of the electrical signal produced by the receptor, termed the receptor potential, are related to the intensity and time course of stimulation of the receptor. The process by which specific stimulus energy is converted into an electrical signal is called stimulus transduction.
Sensory receptors are morphologically specialized to transduce specific forms of energy, and each receptor has a specialized anatomical region where stimulus transduction occurs. Most receptors are optimally selective for a single type of stimulus energy, a property termed receptor specificity. We see particular colors, for example, because we have receptors that are selectively sensitive to photons with specific wavelengths, and we smell particular odors because we have receptors that bind specific odorant molecules (Figure 21–6).
Sensory receptors are specialized to transduce a particular type of stimulus energy into electrical signals.
Sensory receptors are classified as chemoreceptors, photo receptors, or mechanoreceptors depending on the class of stimulus energy that excites them. They transform that energy into an electrical signal that is transmitted along pathways that serve one sensory modality. The insets in each panel illustrate the location of the ion channels that are activated by stimuli.
A. The olfactory hair cell responds to chemical molecules in the air. The olfactory cilia on the mucosal surface bind specific odorant molecules and depolarize the sensory nerve through a second-messenger system. The firing rate signals the concentration of odorant in the inspired air.
B. Rod and cone cells in the retina respond to light. The outer segment of both receptors contains the photopigment rhodopsin, which changes configuration when it absorbs light of particular wavelengths. Stimulation of the chromophore by light reduces the concentration of cyclic guanosine 3', 5'-monophosphate (cGMP) in the cytoplasm, closing cation channels and thereby hyperpolarizing the photoreceptor. (Adapted, with permission, from Shepherd 1994.)
C. Meissner's corpuscles respond to mechanical pressure. The fluid-filled capsule (blue) surrounding the sensory nerve endings (pink) is linked to the fingerprint ridges by collagen fibers. Pressure or motion on the skin opens stretch-sensitive ion channels in the nerve fiber endings, thus depolarizing them. (Adapted, with permission, from Andres and von Düring 1973.)
Human sensory receptors are classified as mechanoreceptors, chemoreceptors, photoreceptors, or thermoreceptors (Table 21–1). Mechanoreceptors and chemoreceptors are the most widespread and the most varied in form and function.
Table 21–1Classification of Sensory Receptors ||Download (.pdf) Table 21–1 Classification of Sensory Receptors
|Sensory system ||Modality ||Stimulus ||Receptor class ||Receptor cells |
|Visual ||Vision ||Light (photons) ||Photoreceptor ||Rods and cones |
|Auditory ||Hearing ||Sound (pressure waves) ||Mechanoreceptor ||Hair cells in cochlea |
|Vestibular ||Head motion ||Gravity, acceleration, and head motion ||Mechanoreceptor ||Hair cells in vestibular labyrinths |
|Somatosensory || || || ||Cranial and dorsal root ganglion cells with receptors in: |
| ||Touch ||Skin deformation and motion ||Mechanoreceptor ||Skin |
| ||Proprioception ||Muscle length, muscle force, and joint angle ||Mechanoreceptor ||Muscle spindles and joint capsules |
| ||Pain ||Noxious stimuli (thermal, mechanical, and chemical stimuli) ||Thermoreceptor, mechanoreceptor, and chemoreceptor ||All tissues except central nervous system |
| ||Itch ||Histamine ||Chemoreceptor ||Skin |
| ||Visceral (not painful) ||Wide range (thermal, mechanical, and chemical stimuli) ||Thermoreceptor, mechanoreceptor, and chemoreceptor ||Gastrointestinal tract, urinary bladder, and lungs |
|Gustatory ||Taste ||Chemicals ||Chemoreceptor ||Taste buds |
|Olfactory ||Smell ||Odorants ||Chemoreceptor ||Olfactory sensory neurons |
Six different kinds of mechanoreceptors that sense skin deformation, motion, stretch, and vibration are responsible for the sense of touch. Muscles contain three kinds of mechanoreceptors that signal muscle length, velocity, and force, whereas other mechanoreceptors in the joint capsule signal joint angle. Hearing is based on two kinds of mechanoreceptors, inner and outer hair cells, that transduce motion of the basilar membrane in the inner ear. Other hair cells in the vestibular labyrinth sense motion and acceleration of the fluids of the inner ear to signal head motion and orientation. Visceral mechanoreceptors detect the distension of internal organs such as the bowel and bladder. Osmoreceptors in the brain, which sense the state of hydration, are activated when a cell swells. Certain mechanoreceptors report extreme distortion that threatens to damage tissue; their signals reach pain centers in the brain.
Chemoreceptors are responsible for olfaction, gustation, itch, pain, and many visceral sensations. A significant part of pain is due to chemoreceptors that detect molecules spilled into the extracellular fluid by tissue injury and molecules that are part of the inflammatory response. Several kinds of thermoreceptors in the skin sense skin warming and cooling. Another thermoreceptor, which monitors blood temperature in the hypothalamus, is mainly responsible for whether we feel warm or cold.
Vision is mediated by four kinds of photoreceptors in the retina. The light sensitivities of these receptors define the visible spectrum. The photopigments in rods and cones detect electromagnetic energy of wavelengths that span the range 390 to 670 nm (Figure 21–7A). Unlike some other species, such as birds or reptiles, humans do not detect ultraviolet light or infrared radiation because we lack receptors that detect the appropriate short or long wavelengths. Similarly, radio waves and microwave energy bands are not perceived because humans have not evolved receptors for these frequencies.
Human perception of colors results from the simultaneous activation of three different classes of photoreceptors in the retina.
A. The visible spectrum of light spans wavelengths of 390 to 670 nm. Individual rod or cone photoreceptors are sensitive to a broad range of wavelengths (black and white curves), but each is most responsive to light in a particular spectral band. As a result, cone photoreceptors are classified as red, green, and blue types. The specific colors perceived result from the relative activation of the three cone types. (Adapted, with permission, from Dowling 1987.)
B. The neural coding of color and brightness in the retina can be portrayed as a three-dimensional vector in which the strength of activation of each cone type is plotted along one of the three axes. Each point in this three-dimensional space represents a unique pattern of activation of the three cone types. The direction of the vector represents the relative activation of the three cone types and the color seen. In the example shown here strong activation of red cones, moderate stimulation of green cones, and weak activation of blue cones produces the perception of yellow. The length of the vector from the origin to the point represents the intensity or brightness of light in that region of the retina.
Multiple Subclasses of Sensory Receptors Are Found in Each Sense Organ
Sensory receptors are found in specialized epithelia called sense organs, principally the eye, ear, nose, tongue, and skin. The arrangement of receptors in an organized structure allows further specialization of function within each sensory system.
Each major sensory system has several constituent qualities or submodalities. For example, taste can be sweet, sour, salty, or bitter; objects that we see differ in color; and touch has qualities of temperature, texture, and rigidity. Submodalities exist because each class of receptors contains a variety of specialized receptors that respond to limited ranges of stimulus energies.
The receptor behaves as a filter for a narrow range or bandwidth of energy. For example, an individual photoreceptor is not sensitive to all wavelengths of light but only to a small part of the spectrum. We say that a receptor is tuned to an optimal or best stimulus, the unique stimulus that activates the receptor at low energy and evokes the strongest response. As a result, we can plot a tuning curve for each receptor based on physiological experiments (the white and black curves in Figure 21–7A). The tuning curve shows the range of sensitivity of the receptor, including its threshold, the minimum stimulus intensity at which the receptor is activated. For example, blue cones in the retina are most sensitive to light of 437 nm; for that reason, they are also termed S or short-wavelength receptors. Green cones, termed M receptors for their sensitivity to middle wavelengths, respond best to 533 nm; red cones, the L or long-wavelength receptors, respond most vigorously to 564 nm wavelengths. The blue, green, and red cones respond to other wavelengths of light but these responses are weaker (see Chapter 26).
The graded sensitivity of photoreceptors means that each rod and cone responds to a wide spectrum of colors yet signals a specific wavelength by the amplitude of the evoked receptor potential. However, because the tuning curve is symmetric around the best frequency, wavelengths of greater or lesser values may evoke identical responses. For example, red cones respond equally well to light of 520 and 600 nm. How does the brain interpret these signals? The answer lies with the green and blue cones. Green cones respond very strongly to light of 520 nm, as it is close to their preferred wavelength, but respond weakly to 600 nm light. Blue cones do not respond to 600 nm light and are barely activated at 520 nm. As a result, 520 nm light is perceived as green, whereas 600 nm is seen as orange. Thus we are able to perceive a spectrum of colors through varying combinations of photoreceptors.
Similarly, the complex flavors we perceive when eating are a result of combinations of chemoreceptors of varying affinities for natural ligands. The broad tuning curves of a large number of distinct olfactory and gustatory receptors afford endless combinatorial possibilities.
Neural Firing Patterns Transmit Sensory Information to the Brain
The receptor potential generated by an adequate stimulus produces a local depolarization or hyperpolarization of the sensory receptor cell. However, the sense organs are located at distances far enough from the central nervous system that passive propagation cannot suffice to convey signals there. To communicate sensory information to the brain a second step in neural coding must occur. The change in membrane potential produced by the sensory stimulus is transformed into action potentials that can be propagated over long distances.
Action potentials are generated in olfactory sensory neurons and dorsal root ganglion neurons of the somatosensory system whose axons project directly to the central nervous system. In the auditory, vestibular, and gustatory (taste) systems the receptor cells make synaptic contact with the peripheral branches of the sensory axons that form cranial nerves VIII, VII, and IX. The retina has the most elaborate neural network for processing sensory information. Photoreceptors send signals through a series of local interneurons to retinal ganglion cells that transform visual information into bursts of action potentials that travel to the brain through the optic nerve.
Sensory receptors encode the intensity of the stimulus in the amplitude of the receptor potential. This analog signal of intensity is transformed into a digital pulse code in which the frequency of action potentials is proportional to the intensity of the stimulus (see Figure 21–3A). The notion of an analog-to-digital transformation dates back to 1925 when Edgar Adrian and Yngve Zotterman discovered the all-or-none properties of the action potential in sensory neurons. Zotterman would later write:
November 2, 1925, was a red letter day for both of us…. We were excited, both of us quite aware that what we now saw had never been observed before and that we were discovering a great secret of life, how the sensory nerves transmit their information to the brain…. We had found that the transmission in the nerve fiber occurred according to impulse frequency modulation (FM) twenty years before FM was introduced in teletechnique.
Despite the rather crude recording instruments available at that time, Adrian and Zotterman discovered that the frequency of firing—the number of action potentials per second—varies with the strength of the stimulus and the time over which it has been in action; stronger stimuli evoked larger receptor potentials that generated a greater number and a higher frequency of action potentials.
In later years, as recording technology improved and digital computers allowed precise quantification of the timing of action potentials, Mountcastle and his colleagues demonstrated a precise correlation between sensory thresholds and neural responses, as well as the parametric relationship between neural firing rates and self-reports of the intensity of sensations (see Figure 21–3). They also found that the dynamics of the spike train conveys important information about fluctuations of the stimulus, such as the frequency of vibration or a change in rate of movement. Humans can report changes in sensory experience that correspond to alterations in the firing patterns of sensory neurons in the range of a few milliseconds.
The temporal properties of a changing stimulus are encoded as changes in the pattern of sensory neuron activity. Many sensory neurons signal the rate at which stimulus intensity changes by rapidly altering their firing rates. For example, in slowly adapting mechanoreceptors the initial spike discharge when a probe touches the skin is proportional to both the speed at which the skin is indented and the total amount of pressure (Figure 21–8A). During steady pressure the firing rate slows to a level proportional to skin indentation. Firing stops when the probe is retracted. Thus, neurons signal important properties of stimuli not only when they fire but also when they stop firing.
Firing rates of sensory neurons convey information about the stimulus intensity and time course.
These records illustrate responses of two different classes of touch receptors to a probe pressed into the skin. The stimulus amplitude and time course are shown in the lower trace of each pair; the upper trace shows the action potentials recorded from the sensory nerve fiber in response to the stimulus.
A. A slowly adapting mechanoreceptor responds as long as pressure is applied to the skin. The total number of action potentials discharged during the stimulus is proportional to the amount of pressure applied to the skin. The firing rate is higher at the beginning of skin contact than during steady pressure, as this receptor also detects how rapidly pressure is applied to the skin. When the probe is removed from the skin, the spike activity ceases. (Adapted, with permission, from Mountcastle, Talbot, and Kornhuber 1966.)
B. A rapidly adapting mechanoreceptor responds at the beginning and end of the stimulus, signaling the rate at which the probe is applied and removed; it is silent when pressure is maintained at a fixed amplitude. Rapid motion evokes a brief burst of high-frequency spikes, whereas slow motion evokes a longer-lasting, low-frequency spike train. (Adapted, with permission, from Talbot et al. 1968.)
The instantaneous firing patterns of sensory neurons are as important to sensory perception as the total number of spikes fired over long periods. Steady rhythmic firing in nerves innervating the skin is perceived as vibration or steady pressure. Bursting patterns may be perceived as motion. If a stimulus persists unchanged for several minutes without a change in position or amplitude, the neural response diminishes and sensation is lost, a condition called receptor adaptation.
Receptor adaptation is thought to be an important neural basis of perceptual adaptation, whereby a constant stimulus fades from consciousness. Receptors that respond to prolonged and constant stimulation, known as slowly adapting receptors, encode stimulus duration by generating action potentials throughout the period of stimulation. In contrast, rapidly adapting receptors respond only at the beginning or end of a stimulus; they cease firing in response to constant amplitude stimulation and are active only when the stimulus intensity increases or decreases (Figure 21–8B).
The existence of two kinds of receptors—rapidly and slowly adapting sensors—illustrates another important principle of sensory coding. Sensory systems detect contrasts in discrete stimuli, changes in the temporal and spatial patterns of stimulation.
The intensity of a stimulus is also represented in the brain by the total number of active neurons in the receptor population. This type of population code depends on the fact that individual receptors in a sensory system differ in their sensory thresholds or in their affinity for particular molecules. Most sensory systems have low- and high-threshold receptors. When stimulus intensity changes from weak to strong, low-threshold receptors are first recruited, followed by high-threshold receptors. Parallel processing in low- and high-threshold pathways extends the dynamic range of a sensory system by overcoming the maximum firing rate of 1,000 spikes per second imposed by the absolute refractory period. For example, rod cells in the retina are activated in very dim light but reach their maximal receptor potentials in daylight. Cone cells do not respond in dim light but sense differences in brightness in daylight. The combination of the two types of photoreceptors allows us to perceive light intensity over several orders of magnitude.
As this discussion illustrates, the possibilities for information coding through temporal patterning within and between neurons in a population are enormous. For example, the timing of action potentials in the presynaptic cell can determine whether the postsynaptic cell fires. Two action potentials that arrive synchronously or nearly so will drive the postsynaptic neuron's membrane potential much further toward or away from the threshold for an action potential than would asynchronous action potentials. The timing of action potentials between neurons also has a profound effect on long-term potentiation and long-term depression at synapses (see Chapter 67).
The Receptive Field of a Sensory Neuron Conveys Spatial Information
Populations of neurons are also important for conveying the spatial properties of stimuli in a variety of modalities. The spatial attributes of visual, tactile, and auditory stimuli include the location, dimensions, shape, and tonal frequency of the stimuli. The spatial attributes of proprioceptive stimuli include the length of muscles, joint postures, and the body's orientation in the gravitational field. These properties are linked to the anatomical arrangement of receptors within each sense organ.
The position of a sensory neuron in the sense organ is a major element of the specific information conveyed by that neuron (Figure 21–9). The skin area or region of space or tonal domain in which stimuli can activate a sensory neuron is called its receptive field. The skin area or region of space from which a sensation seems to arise is called the neuron's perceptive field. The two usually coincide.
The receptive field of a sensory neuron is the spatial domain in the sense organ where stimulation excites or inhibits the neuron.
The receptive field of a touch-sensitive neuron denotes the region of skin where gentle tactile stimuli evoke action potentials in that neuron. It encompasses all of the receptive endings and terminal branches of the sensory nerve fiber. If the fiber is stimulated electrically with a microelectrode, the subject experiences touch localized to the receptive field on the skin. The area from which the sensation arises is called the perceptive field. A patch of skin contains many overlapping receptive fields, allowing sensations to shift smoothly from one sensory neuron to the next in a continuous sweep. The axon terminals of sensory neurons in the central nervous system are arranged somatotopically, providing an orderly map of the innervated region of the body.
The dimensions of receptive fields play an important role in the ability of a sensory system to encode spatial information. The objects that we see with our eyes or hold in our hands are much larger than the receptive field of an individual sensory neuron, and therefore stimulate groups of adjacent receptors. The size of the stimulus therefore influences the total number of receptors that are activated. In this manner the spatial distribution of active and silent receptors provides a neural image of the size and contours of the stimulus. This pattern is called an isomorphic representation of the stimulus.
Each receptor in the active population encodes the type of energy applied to the receptive field, the local stimulus magnitude, and its temporal properties. For example, auditory codes describe the tonal frequency, loudness, and duration of sound-pressure waves hitting the ear, whereas visual codes describe the hue, brightness, and time course of light hitting the retina. The neural representation of an object or scene is therefore composed of a mosaic of individual receptors that collectively signal its size, contours, texture, color, and temperature.
A good way to visualize the neural activity of a population of neurons, and to grasp the range of possibilities for population coding, is to think of neurons as points in a visual display that flash brightly whenever an action potential occurs. If the action potentials occur at random times, one would perceive a disorganized pattern of flickering dots like the "snow" on old-style television screens without a signal. However, if groups of pixels are turned on and off synchronously, coherent spatial patterns appear. Similarly, when a horizontal bar of light stimulates a row of adjacent photoreceptors in the retina, action potentials are generated in neighboring ganglion cells. Although each photoreceptor simply registers light in its receptive field, the pattern of a bar emerges from the population of active ganglion cells. Neurons in the central nervous system decipher the image of a bar by responding preferentially to specific ensembles of active receptors.
Synchronous patterns of activity in sensory neuron populations convey the spatial dimensions of the stimulus but do not in themselves signal its intensity. The brightness and contours of a video image are created by modulation of the luminance of each pixel. Similarly, in neural codes signal strength is conveyed by the impulse rates of the individual neurons. This is called rate coding. The temporal integration of action potentials that occurs at synapses smooths the staccato on-off firing patterns into a continuous modulated signal analogous to the gray scale of a video monitor. High firing rates in this model yield white zones, intermediate rates produce gray zones, and silence gives a black region. Rate coding thereby allows the population of neurons to simultaneously transmit the spatial properties and intensity of stimuli.
The spatial resolution of a sensory system is proportional to the total number of receptor neurons and how their receptive fields are apportioned within the population (Figure 21–10). Regions of a sense organ with a high density of receptors, such as the central retina (the fovea), have small receptive fields because the terminals of each sensory neuron are confined to a local cluster of receptors. Each retinal ganglion cell in the fovea measures the average light intensity in a small spot of the visual field; but because there are so many of them, the population of cells in the fovea transmits a very detailed representation of the visual scene. Ganglion cells in the periphery of the retina have larger receptive fields because the receptor density is much lower. The dendrites of each ganglion cell receive information from a wider area of the retina, and thereby integrate light intensity over a greater portion of the visual field. This arrangement yields a less detailed image of the scene (Figure 21–10A). Similarly, the region of the body most often used to touch objects is the hand. Not surprisingly, mechanoreceptors for touch are concentrated in the fingertips, and the receptive fields on the hand are smaller than those on the arm or trunk.
The spatial properties of scenes and objects are conveyed by populations of neurons, each of which represents a small component of the image.
The resolution of detail is inversely correlated with the area of the receptive field of individual neurons. Each square or pixel in these images represents a receptive field. The gray scale in each pixel is proportional to the average light intensity in the corresponding receptive field. If there are a small number of neurons, and each spans a large area of the image, the result is a very schematic representation of the scene (A). As the density of neurons increases, and the size of each receptive field decreases, the spatial detail becomes clearer (B, C). The increased spatial resolution comes at the cost of larger populations of neurons required to transmit the information. (Photographs reproduced with permission of Daniel Gardner.)
Spatial coding is ubiquitous for two reasons. First, it takes advantage of the parallel architecture of the nervous system. The number of neurons in each unimodal area of sensory cortex is approximately 100 million. Thus the possible number of spatial patterns of neural activity greatly exceeds the number of atoms in the universe. Second, each neuron is a spatial as well as a temporal decoder: It fires only when many of its excitatory synapses receive action potentials and most of the inhibitory synapses do not. That is, it fires in response to some patterns of stimulation and not others. The fact that on average each cortical neuron has 10,000 synapses makes the number of spatial coding possibilities enormous.
Spatial codes are sometimes called vector codes from the mathematical idea of vector spaces. The firing rate of each neuron in a population can be plotted in a coordinate system with multiple axes such as modality, location, intensity, and time. The neural components along these axes combine to form a vector that represents the population's activity (see Figure 21–7B). The vector interpretation is useful because it makes available powerful mathematical techniques.
The fragmentation of a stimulus into components, each encoded by an individual neuron, is the initial step in sensory processing. Assembly of the components into an internal representation of an object occurs within neural networks in the brain. This process allows the brain to abstract certain features of an object, person, scene, or external event from the detailed receptor input. As a result, the internal representation formed in the brain may exaggerate some features that are important at the moment while ignoring others. In this sense our percepts are not perfect mirrors of the stimuli that evoke them but instead a creation of the mind.