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Sensory Systems
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The Senses and Quantifying Percept
Sensory Responses at the Cellular Level
References
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The Senses and Quantifying Percept
The Greek literature of Homer, spoke of hearing and seeing yet, there was no word, such as ‘sensation’ or ‘perception’ that could
sum up the different features of hearing or sight. The word ‘aesthesis’ originated around the fifth century B.C. and was used by both
Aristotle and Plato to mean sensation or perception; however, there was no definitive proof that philosophers had a concept of the
word (Hamlyn, 1961). Alcmaeon of Croton, a physiologist of the pre-Socratic period who viewed the brain as the common
sensorium, was one of the earliest theorists of sensation and perception. Theophrastus (ca. 372–286 B.C.), a colleague of Aristotle,
writes in ‘De Sensu’ that Alcamaeon viewed perception to be the effect of unlike upon unlike; he distinguished between sensation
and perception (Kirk and Raven, 1957). Like Alcamaeon, Anaxagoras (ca. 500–428 B.C.) supported this same theory by pointing
out that objects of the same temperature as ourselves neither warm nor cool us on their approach. The effect of unlike upon unlike
was a kind of pain that was perceived by the sense organs only when excessive in duration or intensity. The atomists of the
pre-Socratic period, Leucippus (ca. fifth century B.C.) and Democritus (ca. 460–370 B.C.), took this concept a step further. They
postulated that sense-perception ‘arises when atoms given off by bodies in the form of the effluences make contact with the atoms
of the soul, which pervade the whole body, including the sense organs’ (Hamlyn, 1961).
Plato (c.a. 428–347) and Aristotle (c.a. 384–322) dealt with epistemological issues and how sense perception is important to
this concept. Plato made a distinction between knowledge, ignorance, and the intermediate state of opinion. He suggests that
"aesthesis" is knowledge and cites a causal theory of perception, in that perception occurs as a result of the meeting of motions from
the eye and motions from the object, resulting in both perception and the perceived object. In comparison, Aristotle viewed the
heart as the seat of the senses and perception as both an active and passive sense. In his view, the sense or sense organ receives a
"quality" of the object and is potentially what the object is in reality. There are three important points associated with this idea: 1)
each sense has a "special" object (i.e., hearing has sound, smell has odor, etc.), 2) there are certain qualities associated with objects,
but not necessarily with the special sense, 3) that which we see or feel is to be identified in a particular way.
The philosophy of sensation and perception in the Hellenistic period was more concerned with nature and a person’s place in it,
rather than dealing with theories of knowledge. Epicurus (c.a. 341–271) suggested that everything was composed of atoms, and
that sense perception is the result of direct contact with atoms of the soul. The Stoics believed perception as being a change
(apathos) in the soul that reflects the nature of the object being perceived. In comparison, Plotinus (204–270 C.E.), the founder of
Neo-Platonism, reverted back to the philosophy of Plato, in which the soul actively functions in perception but impressions are left
on the body rather than the soul. Plotinus served as the connection between the Greeks and the Middle Ages, where sensation and
perception was more concerned with theological issues. St. Augustine suggested that an object making contact with the sense organ
is merely a prelude to sensation. Accordingly, "sensation occurs when the soul becomes actively recipient of the impression received
from its messenger the sense" (Ledvina, 1941). In comparison, St. Thomas Aquinas’ thinking was along the lines of combining
ideas from the atomists and Aristotle (Hamlyn, 1961).
It was not until the seventeenth century that Descartes ushered in a new era of thought with the idea of ‘method,’ suggesting that
truth can be found by devising a method. This idea was one of the presuppositions of philosophical thinking in the seventeenth
and eighteenth centuries and is the basis for the later development of psychophysics and the measurement of sensation. Descartes
believed that perceiving and sensation are modes of the mind, but there are physical and physiological processes underlying these
modes that result in the mind having ideas (Smith and Grene, 1956). Reactions to Descartes’ ideas influenced the British school of
empiricism in the seventeenth and eighteenth centuries, which included Locke, Hume, and Berkeley. Their theory of knowledge
saw the sense experience as the sole source contributing to knowledge. Locke postulated that ideas are produced in our minds by
things that are outside of us. His ideas, such as those on primary and secondary object qualities, were in some respects similar to
those of Aristotle (Hirst, 1965).
Among the first to make a quantitative statement concerning sensation was Krüger (1743), who proposed that sensation
increases proportionally in its strength with increases in stimulus strength. Yet, it was Luigi Galvani’s published work in 1791, on
the contractions of frog muscles and ‘animal electricity,’ that served as the impetus for Helmholtz, Müller, and Weber to test
hypotheses by measuring ‘specific nerve energies.’ Weber showed in 1834 that the ability to discriminate the difference between
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Change History: August 2014. BHA Sokolowski Additions to sections on adaptation, spatial arrangement and topology. References updated and added
Figure 1.
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Sensory Systems
standard and comparison weights was not absolute but, rather, depended on the ratio of the magnitude of one weight to its
standard. For example, one can readily determine the difference between 1 and 2 kg as opposed to 61 and 62 kg. His second
experiment involved the sense of touch. If the tips of two pins touch the skin at two adequately separated points (stimuli), one
would report sensing two different points of contact. If the distance between the pins is decreased, a distance would be reached
where one would feel only the pressure of one point, although both tips are applied. This distance would later be known as the
two-point threshold or ‘limen.’ These studies were among the first psychological experiments, since they measured discrimination.
The relationship, later written as Weber’s Law,
Df ¼ Cf
was described as the amount by which the intensity of a stimulus must be increased or decreased (Df) in order for a sensory change
to be detected is a constant fraction (C) of the original stimulus intensity (f).
Fechner, the father of psychophysics, was interested in measuring mental energy in relation to physical energy and extended
Weber’s law in 1860. Using the idea of the just noticeable difference (JND), or ‘limen,’ he proposed that, if one increased the
magnitude of the JND in an arithmetical order (i.e., 1, 2, 3, 4, 5, . . .), the actual physical magnitude to produce the JND increased in
a geometrical order (i.e., 1, 2, 4, 8, 16, . . .). This concept, known as Fechner’s logarithmic law, was written as
C ¼ k log f=b
where C is the perceived sensation magnitude or intensity, f is stimulus intensity, b is the stimulus intensity at absolute threshold,
and k is a constant of proportionality (Fechner, 1860).
An outgrowth of Fechner’s research was further debate and alternatives to his law, resulting in various methodological
treatments and the development of psychometric scales. In the 1950s, Stevens (1953, 1957) proposed a psychophysical power
law, which states ‘equal stimulus ratios produce equal sensation ratios.’ This relationship was written as:
log C ¼ blog fbk
where C represents the perceived sensation of intensity, f is the stimulus intensity, and b and k, the exponents, are the stimulus
intensity at absolute threshold and the constant of proportionality, respectively. The power law for perceived sensation holds for
many sensory data and, interestingly, finds support among sensory neuronal responses (Stevens, 1970).
Sensory Responses at the Cellular Level
As far back as ancient times, sensory systems have been divided into five sensory modalities: hearing, smell, taste, touch, and vision.
Others have been recognized and fall within the somatovisceral category that previously included touch (mechanoreception) and
more recently, position and movement (proprioception), heat and cold (thermoreception), and pain (nociception) (Gebhart,
1995) (Table 1). While we may typically think of sensation as originating in the external world (exteroceptive), there are sensations
that originate internally (interoceptive). This internal sensory information, which arises from the viscera, blood vessels, and
muscles and is used to regulate body temperature, heart and respiratory rate, and blood pressure, may not be recognized at a
conscious level.
Table 1
Sensory systems, modalities, and cell types
Sensory
systems
Visual
Auditory
Vestibular
Somatosensory
Gustatory
Olfactory
Modality
Stimulus
Receptor types
Receptor cell-types
Vision
Hearing
Balance
Somatic
senses:
Touch
Light
Sound
Motion, gravity
Photoreceptors
Mechanoreceptor
Mechanoreceptor
Rods, cones, ganglion cells
Hair cells
Hair cells
Dorsal root ganglion neurons
Pressure
Mechanoreceptor
Proprioception
Temperature
sense
Pain
Displacement
Thermal
Mechanoreceptor
Thermoreceptor
Cutaneous mechanoreceptor, dorsal root
ganglion neurons
Muscle and joint receptors
Cold and warm receptors
Chemical, thermal,
mechanical
Chemical
Chemical
Chemical
Chemoreceptor, thermoreceptor,
mechanoreceptor
Chemoreceptor
Chemoreceptor
Chemoreceptor
Polymodal, thermal, and mechanical
nociceptors
Chemical nociceptor
Taste buds
Olfactory sensory neurons
Itch
Taste
Smell
Modified from Kandel et al. (2000) Principles of Neural Science, McGraw-Hill, New York, NY. p. 414
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Each sensory system begins with a receptor cell and its primary afferent neuron that makes specific connections with other nerve
fibers. The groups of neuronal fibers and the nuclei that relay this peripheral information into and throughout the central nervous
system define the sensory system. These neurons are essentially tuned to a specific sensory energy. It is this specificity that defines
the sensation. A demonstration of this phenomenon would be to replace a peripheral sensory endorgan with an artificial device.
The outcome, when using such a device, is nicely demonstrated in deaf patients who receive a cochlear implant. Here, the implant
electrically stimulates the peripheral ganglion cells that relay the electrical information to the central auditory system, producing
the sensation of sound in the patient.
While it generally has been accepted that all sensory stimulation begins with a specialized receptor cell, data over the last decade
have overturned this dogma. In the visual system, for example, evidence shows that there is a small group of nerve cells that are
extraocular receptors. These intrinsically photosensitive Retinal Ganglion Cells (ipRGCs) contain melanopsin, a photopigment,
thus rendering these cells as a third class of photoreceptor in addition to rods and cones. Initial studies suggested these cells were
involved with the circadian rhythm, based on their neural projections, however, more recent data suggest some contribution to
vision, as in judging spatial brightness (see Lucas, 2013, for review). A second example is the piezo channels, which are mechanically
activated cation channels in dorsal root ganglion cells (Coste et al., 2010) that have a role in carrying the sense of touch and pain.
The initiation of a receptor response is dependent on an adequate stimulus, as defined by Sherrington (1900), in which a
specific stimulus is needed to initiate a response in a specific sensory receptor. The process, by which a sensory stimulus is converted
into electrochemical energy, occurs at the level of the receptor cell and is known as transduction. This conversion of energy allows
the sensory stimulus to be coded by the peripheral and central nervous systems. For example, in hearing (bending of stereocilia)
and touch (deformation of Pacinian corpuscles), mechanical energy is converted into current as ions flow down their concentration
gradient (electrochemical) through mechanically-gated pores (i.e., ion channels) in the membrane. This flow of current generates
cell membrane potentials known as receptor potentials. The initiation of a response is dependent on four factors: modality,
intensity, location, and timing. As stated above, in relation to specificity, the type of stimulus energy (sound, light, etc.) and the
specificity of the receptors needed to sense that energy defines the modality. The intensity of a perceived stimulus at the cellular
level is reflected in how long and fast the neurons fire, and how many neurons in a population are firing. Thus, timing plays a role
in this process, since an increase in stimulus rate results in an increase in firing rate, while an increase in stimulus amplitude results
in an increase in receptor potential. Interestingly, for some sensory systems, there is a close relationship between the subjective
measurement of intensity, as defined by perception, and the objective measurement, as defined by the neuronal response; both
types of responses can be described by the power function proposed by Stevens (1957) from his psychophysical experiments.
However, this response is not strictly linear. For example, measurements of basilar membrane displacement in the cochlea in
response to sound (Le Page and Johnstone, 1980; Rhode and Robles, 1974), or the measurement of an FA receptor’s response to
touch on the skin (Vallbo and Johansson, 1984), show a stimulus-response relationship that is non-linear. Moreover, inherent in
the response is the intensity threshold necessary to activate the receptor and, eventually, the sensation. For example, what is the
lowest stimulus at which an individual can perceive a specific sound frequency? At the cellular level, the threshold is defined by the
sensitivity of the receptor and the neuronal cells. Stimulation of the receptor cells occurs at a local level and is the result of a passive
flow of ions (e.g., K+, Ca2+, Na+) down a concentration gradient. Stimulation of the neurons is dependent on reaching the threshold
necessary to generate an action potential in the many neurons that encode and relay the signal to and throughout the central
nervous system. The generation of action potentials will generate a sensation depending on the strength of the stimulus.
Once a response is initiated, a change in stimulus is necessary to maintain a receptor cell response and the perceived sensation.
However, if a stimulus remains constant over time, the receptor cell response undergoes a process known as adaptation, resulting in
a decrease in the receptor potential and, thus, a decrease in sensation. A common example of this phenomenon is when one enters
a room with a bad odor. Over time this percept changes, so that the odor sensation is less intense. In the olfactory system,
adaptation is a function of changes in intracellular signals that change with time so that the system undergoes immediate, short and
long-term adaptation as a consequence of increased calcium. Initially, this can involve the binding of a calcium-binding protein
(CBP) that desensitizes a cyclic nucleotide-gated (CNG) channel. With increased calcium, it involves the desensitization of an
adenylyl cyclase, via a calcium calmodulin cyclase, leading to a decrease in the cyclic adenosine monophosphate (cAMP) that
activates the CNG channel. Finally, over more time, it can result in the activation of a carbon monoxide/cyclic guanosine
monophosphate (CO/cGMP) signalling pathway, which inhibits the cyclic nucleotide-gated channel. All of this occurs after the
odorant binds to a receptor that is bound to a G-protein. This binding releases the a subunit of an olfactory G-protein (Golf ) to
activate adenylyl cyclase to produce cAMP, which causes the influx of calcium and sodium by opening the CNG channel and
depolarizing the cell. Calcium influx also binds to a calcium-activated chloride channel that further depolarizes the cell. However,
with increased calcium the system undergoes the steps in adaptation described above and also shown in Figure 1. The cell is
eventually brought to homeostasis via a calcium/sodium exchanger.
Another example of adaptation occurs in the receptor cells (i.e., hair cells) of the auditory system, where bending of stereocilia
(Figure 2) results in the stretching of tip links or filaments that open mechano-sensitive transduction (MeT) channels, resulting in
receptor cell depolarization/excitation. Bending of the stereocilia with a constant force results in a decrease in tip link tension by a
mechanical mechanism involving the proteins actin and myosin (Hudspeth and Gillespie, 1994; Peng et al., 2011). As the
stereocilia are bent, the myosin motor moves up and down actin filaments in the stereocilia to either increase or decrease tip
link tension, which resets the MeT channel to a resting state. The sensory cell, via the transduction channel, is now able to respond
to any new change in stimulus. Adaptation can take place either slowly or rapidly, as demonstrated also in touch receptors. Through
the process of adaptation, the receptors and neurons can encode and convey the ever-changing sensory signals to the brain.
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Figure 1 An illustration of (1) immediate, (2) short, and (3) long-term adaptation in the olfactory system.
Figure 2 An illustration of structures used during adaptation in receptor or hair cells of the cochlea.
A feature of sensory systems that contributes to their specificity is their spatial arrangement. This arrangement contributes to the
localization of a stimulus and to the ability to discern the physical characteristics of that stimulus (e.g., size, shape, frequency, etc.).
For example, touch receptors in the fingertips and lips occur in clusters, offering a more stimulus sensitive arrangement than
receptors in the back of the hand, which are less clustered and more randomly organized. In the gustatory system, receptors for taste
that are most sensitive to salts, acids, bases, sugars, proteins, and fatty acids are arranged on different parts of the tongue. In the
auditory system, the basilar membrane of the cochlea is tonotopically organized, responding in a low to high frequency
arrangement along its length, from apex to base, respectively. This organization is the result of its physical characteristics; it is
thin and wide at the apex and thick and narrow at the base. Consequently, a low frequency tone of 20 Hz maximally stimulates this
membrane near the apical end, whereas a frequency of 20 kHz maximally stimulates the membrane at the basal end. In turn, the
receptor cells that overlie these regions and transduce this mechanical energy into electrochemical energy are maximally stimulated
as a result of this displacement.
The spatial arrangement of receptor cells in their various sheets of epithelia defines the region whereby an adequate stimulus
excites a particular receptor. For example, a touch receptor has a defined area or receptive field in the skin within which a stimulus
excites the cell. In the cochlea, the basilar membrane and, thereby, the overlying receptor cells are maximally stimulated or tuned to
some specific frequency (best frequency) due to the tonotopic arrangement. The intensity threshold at the best frequency will be
low for a receptor response. However, excitation still occurs at frequencies above or below the best frequency, although, a greater
intensity (higher threshold) is needed to activate the receptor (Figure 3). In the same vein, while certain parts of the tongue (e.g.,
fungiform papilla) might be most sensitive to a particular tastant (e.g., salt), they still respond to other tastants (e.g., sweet, sour).
The spatial arrangement at the sensory periphery is maintained by the neurons that relay information to the cerebral cortex.
Probably the best know is the primary somatosensory cortex, which contains a map of sensory space for touch known as the sensory
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Figure 3 An example of the responses in a single auditory nerve fiber to different pure tone frequencies. This ‘tuning curve’ shows the receptive field of
the fiber to these different frequencies.
homunculus. Here, different parts of the body are represented in distinct regions of the cortex. Another example is the auditory system
of mammals, where the first order neurons or auditory ganglion cells innervate a specific receptor cell that overlies a specifically tuned
region of the basilar membrane. As the auditory neuron leaves the cochlea, each fiber lies adjacent to nerves innervating neighbouring
regions, one with a higher and the other with a lower frequency specificity. Thus, each fiber relays information from a specific
frequency region. This specificity can be seen in electrical recordings from individual neuronal fibers, which show that each VIIth nerve
fiber is tuned, or is most sensitive to, a specific or best frequency. As this information ascends to the cortex, via higher order neurons in
the CNS, the tonotopic information is maintained throughout any given auditory nucleus. Tonotopy within any given set of neuronal
nuclei is also demonstrated in electrical recordings from the brainstem, midbrain, and cortex, where cells within nuclei maintain
distinct frequency selectivity. Thus, the frequency map at the periphery is maintained centrally. For the gustatory system, tastants such
as bitter, sweet, salty, sour, and umami have functional maps that are spatially segregated in the gustatory cortex (Chen et al., 2011).
In vision, there are columns of cells in the visual cortex that predominantly receive information from the visual hemifields of the right
and left eye (Hubel and Wiesel, 1968). Thus, various sensory systems maintain a topographic map, whereby the strictly ordered
relationship with neighbouring neurons at the periphery is maintained centrally.
For some systems, mapping the spatial topology can be more complex. An example is the sense of smell, where it is more
difficult to decipher the underlying mechanisms of chemotopic or odotopic coding. A recent study suggests that humans are able to
distinguish over a trillion different odors (Bushdid et al., 2014). In the olfactory system, however, there are approximately 1000
genetically distinct odor receptors that are spatially arranged into four different regions of the olfactory epithelium in the nasal
septum (Sullivan et al., 1996). Receptors from a specific gene family send their axons to a specific glomerulus in the olfactory bulb,
so that thousands of axons converge on this single structure. Functional studies suggest there is some spatial arrangement in the
bulb based on the chemistry of the odorant, such as carbon length, molecule size, and water solubility ( Johnson and Leon, 2007).
In addition, molecule vibration may also play a role in discrimination (Gane et al., 2013). However, different receptors may analyse
different features of a single odorant. How these are spatially mapped in the brain is still not fully understood. Interestingly, both
odor and taste integrate in specific parts of the human brain such as the insula/operculum, anterior cingulate gyrus, and
orbitofrontal cortex (Small and Prescott, 2005).
The information that is relayed to and integrated in the nuclei of the CNS is complex as different stimulus features are decoded
by the peripheral sense organs. Sensory signals are contrasted and refined through the divergence of fibers to multiple regions of a
nucleus or through the convergence of multiple synapses on a single cell or group of cells. Included in this process are inhibitory
neurons that contribute to functions such as localizing a low frequency stimulus in hearing, regulating selective attention in vision,
or inhibiting information in neighbouring olfactory glomeruli. In addition, fibers within a particular sensory pathway decussate so
that information is shared with both sides of the brain. This sharing of signals can be a part of the integration process, as in sound
localization, in which excitation is maintained on one side of the brain stem, while inhibition is activated on the other side. Also,
the crossing-over of fibers can provide redundancy in some systems so that damage in a part of the pathway may have less severe
effects overall. Finally, the brain itself can contribute in the regulation and integration of sensory stimuli by sending signals back
out to the periphery. We regulate our eye movements in response to different stimuli and our head in response to different sounds,
using various muscles. At the cellular level, studies of the inner ear show that efferent projections, originating in the brain stem and
synapsing on specialized receptor cells of the cochlea, known as outer hair cells, can regulate and contribute to the dynamics of
auditory signal processing. Thus, we are not passive receptors of sensation, but active interlopers in processing sensory information
as we form percepts of our external environment.
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