How humans perceive and understand real-world scenes is a long-standing question in neuroscience, cognitive psychology, and artificial intelligence. Initially, it was thought that scenes are constructed and represented by their component objects. An alternative view proposed that scene perception starts by extracting global features (e.g., spatial layout) first and individual objects in later stages. A third framework focuses on how the brain not only represents objects and layout but how this information combines to allow determining possibilities for (inter)action that the environment offers us. The discovery of scene-selective regions in the human visual system sparked interest in how scenes are represented in the brain. Experiments using functional magnetic resonance imaging show that multiple types of information are encoded in the scene-selective regions, while electroencephalography and magnetoencephalography measurements demonstrate links between the rapid extraction of different scene features and scene perception behavior. Computational models such as deep neural networks offer further insight by how training networks on different scene recognition tasks results in the computation of diagnostic features that can then be tested for their ability to predict activity in human brains when perceiving a scene. Collectively, these findings suggest that the brain flexibly and rapidly extracts a variety of information from scenes using a distributed network of brain regions.
Clemens G. Bartnik and Iris I. A. Groen
John S. Hernandez, Tariq M. Brown, and Karla R. Kaun
The ability to sense and respond to a rewarding stimulus is a key advantage for animals in their natural environment. The circuits that mediate these responses are complex, and it has been difficult to identify the fundamental principles of reward structure and function. However, the well-characterized brain anatomy and sophisticated neurogenetic tools in Drosophila melanogaster make the fly an ideal model to understand the mechanisms through which reward is encoded. Drosophila find food, water, intoxicating substances, and social acts rewarding. Basic monoaminergic neurotransmitters, including dopamine (DA), serotonin (5-HT), and octopamine (OA), play a central role in encoding these rewards. DA is central to sensing, encoding, responding, and predicting reward, whereas 5-HT and OA carry information about the environment that influences DA circuit activity. In contrast, slower-acting neuromodulators such as hormones and neuropeptides play a key role in both encoding the pleasurable stimulus and modulating how the internal environment of the fly influences reward sensation and seeking. Recurring circuit motifs for reward signaling identified in Drosophila suggest that these key principles will help elucidate understanding of how reward circuits function in all animals.
Roswitha Wiltschko and Wolfgang Wiltschko
The magnetic field of the earth provides birds with navigational information, with birds having two different receptor systems, one for the direction, the other for the intensity of the geomagnetic field. The direction of the geomagnetic field is used as a compass, with the avian magnetic compass being an inclination compass not recording the polarity of the field. The respective directional information is perceived by light-dependent radical pair processes in the eyes, with cryptochrome, a photopigment with the chromophore flavin adenine dinucleotide as receptor molecule. It is transmitted by the optic nerve to the brain, where it is processed by parts of the visual system. The magnetic compass not only serves to orient avian flights but also acts as a reference system for route reversal, calibrating the astronomical compass systems, and in migratory birds, as reference for the innate information on the migratory direction. Magnetic intensity and inclination that show gradients from the poles to the magnetic equator are part of the mechanisms that allow birds to determine their position. Intensity is perceived by receptors based on magnetite, a permanently magnetic material. The effect of a brief, strong magnetic pulse and its duration indicates that superparamagnetic particles are involved. The respective information is transmitted by the ophthalmic branch of the trigeminal nerve to the trigeminal brainstem complex in the brain. Testing birds in magnetic fields of a distant site, i.e., magnetically simulating a displacement, documents that magnetic intensity and inclination are very most important components of the navigational “map” that enables birds to determine their position relative to the goal and thus derive the compass course leading to this goal. Furthermore, certain magnetic conditions act as signposts and elicit specific spontaneous responses.
Sensory perceptions are inherently subjective, being influenced by factors such as expectation, attention, affect, and past experiences. Nowhere is this more commonly experienced than with the perception of pain, whose perceived intensity and emotional impact can fluctuate rapidly. The perception of pain in response to the same nociceptive signal can also vary substantially between individuals. Pain is not only a sensory experience. It also involves profound affective and cognitive dimensions, reflecting the activation of and interactions among multiple brain regions. The modulation of pain perception by such interactions has been most extensively characterized in the context of the “descending pain modulatory system.” This system includes a variety of pathways that directly or indirectly modulate the activity of neurons in the spinal dorsal horn, the second-order neurons that receive inputs directly from nociceptors. Less understood are the interactions among brain regions that modulate the affective and cognitive aspects of pain perception. Emerging data suggest that certain pain conditions result from dysfunction in pain modulation, suggesting that targeting these dysfunctions might have therapeutic value. Some therapies that are thought to target pain modulation pathways—such as cognitive behavior therapy, mindfulness-based stress reduction, and placebo analgesia—are safer and less expensive than pharmacologic or surgical approaches, further emphasizing the importance of understanding these modulatory mechanisms. Understanding the mechanisms through which pain modulation functions may also illuminate fundamental mechanisms of perception and consciousness.
Thomas J. Park
Naked mole-rats are subterranean mammals that are native to equatorial east Africa including Ethiopia, Somalia, and Kenya. They are unusual among subterranean mammals in that they live in very large colonies where many respiring animals deplete oxygen and overproduce carbon dioxide. Some of their sensory traits, such as poor vision and hearing, are considered typical of subterranean mammals. However, naked mole-rats display three sensory traits that are unusual even among subterranean mammals. First, they possess a sensitive sensory array of body vibrissae on their otherwise furless bodies. Second, they have a greatly reduced sense of inflammatory and chemical pain, but express acute mechanical and thermal pain. Third, naked mole-rats, and likely other African mole-rat species, are the only rodents known that show no postbirth growth of the vomeronasal organ, an organ associated with sensing pheromones. These sensory traits, along with extreme tolerance to hypoxia and resistance to cancer, make the naked mole-rat an important animal model for studying sensory systems as well as in multiple other scientific fields.
Sandra M. Garraway
Understanding of the various types of plasticity that occur in the spinal cord, as well as understanding of spinal cord functions, has vastly improved over the past 50 years, mainly due to an increase in the number of research studies and review articles on the subject. It is now understood that the spinal cord is not merely a passive conduit of neural impulses. Instead, the spinal cord can independently execute complex functions. Numerous experimental approaches have been utilized for more targeted exploration of spinal cord functions. For example, isolating the spinal cord from supraspinal influences has been used to demonstrate that simple forms of learning can be performed by spinal neuronal networks. Moreover, reduced preparations, such as acute spinal cord slices, have been used to show that spinal neurons undergo different types of modulation, including activity-dependent synaptic modification. Most spinal cord processes, ranging from integration of incoming sensory input to execution of locomotor outputs, involve plasticity. Nociceptive processing that leads to pain and spinal learning is an example of plasticity that is well-studied in the spinal cord. At the neural level, both processes involve an interplay of cellular mediators, which include glutamate receptors, protein kinases, and growth factors. The neurotrophin brain-derived neurotrophic factor (BDNF) has also been implicated in these processes, specifically as a promoter of both pro-nociception and spinal learning mechanisms. Interestingly, the role of BDNF in mediating spinal plasticity can be altered by injury. The literature spanning approximately 5 decades is reviewed and the role of BDNF is discussed in mediating cellular plasticity underlying pain processing and learning within the spinal cord.
Giuliano Gaeta, Regina M. Sullivan, and Donald A. Wilson
Odor- or chemical-guided behavior is expressed in all species. Such behavioral responses to odors begin with transduction at olfactory receptors and, after initial processing in early stages of the olfactory system (e.g., vertebrate olfactory bulb, invertebrate antennal lobe), the information is rapidly (within one to two synapses) distributed to diverse brain regions controlling hedonics, metabolic balance, mating, and spatial navigation, among many other basic functions. Odors can not only drive or guide specific behavioral responses but can also modulate behavioral choices and affective state, in many cases in humans without conscious awareness. Many of the specific neural circuits underlying odor-guided behaviors have been partially described, though much remains unknown. Neural processes underlying odor-guided reward and aversion, kin recognition, feeding, orientation, and navigation across diverse species have been discussed, as well as odor modulation of human behavior and emotion.
Adam Hockley and Susan E. Shore
Tinnitus is the perception of sound that is independent from an external stimulus. Despite the word tinnitus being derived from the Latin verb for ring, tinnire, it can present as buzzing, hissing, or clicking. Tinnitus is generated centrally in the auditory pathway; however, the neural mechanisms underlying this generation have been disputed for decades. Although it is well accepted that tinnitus is produced by damage to the auditory system by exposure to loud sounds, the level of damage required and how this damage results in tinnitus are unclear. Neural recordings in the auditory brainstem, midbrain, and forebrain of animals with models of tinnitus have revealed increased spontaneous firing rates, capable of being perceived as a sound. There are many proposed mechanisms of how this increase is produced, including spike-timing-dependent plasticity, homeostatic plasticity, central gain, reduced inhibition, thalamocortical dysrhythmia, and increased inflammation. Animal studies are highly useful for testing these potential mechanisms because the noise damage can be carefully titrated and recordings can be made directly from neural populations of interest. These studies have advanced the field greatly; however, the limitations are that the variety of models for tinnitus induction and quantification are not well standardized, which may explain some of the variability seen across studies. Human studies use patients with tinnitus (but an unknown level of cochlear damage) to probe neural mechanisms of tinnitus. They use noninvasive methods, often recoding gross evoked potentials, oscillations, or imaging brain activity to determine if tinnitus sufferers show altered processing of sounds or silence. These studies have also revealed putative neural mechanisms of tinnitus, such as increased delta- or gamma-band cortical activity, altered Bayesian prediction of incoming sound, and changes to limbic system activity. Translation between animal and human studies has allowed some neural correlates of tinnitus to become more widely accepted, which has in turn allowed deeper research into the underlying mechanism of the correlates. As the understanding of neural mechanisms of tinnitus grows, the potential for treatments is also improved, with the ultimate goal being a true treatment for tinnitus perception.
Alfredo Fontanini and Lindsey Czarnecki
The gustatory system has evolved to detect molecules dissolved into the saliva. It is responsible for the perception of taste and flavor, for mediating the interaction between perception and internal homoeostatic states, and for driving ingestive decisions. The widely recognized five basic taste categories (sweet, salty, bitter, sour, and umami) provide information about the nutritional or potentially harmful content in what is being consumed. Sweetness is typical of sugars that are carbohydrate dense; saltiness is the percept of ions which are necessary for physiological function and electrolytic homeostasis; bitterness is associated with alkaloids and other potential toxins; sourness is the percept of acidity signaling spoiling foods; and umami is the sensation associated with amino acids in protein-rich foods. In addition to taste, the act of eating also engages sensations of temperature, texture, and odor—the integration of all these sensations leads to the unitary percept of flavor. These same senses, and others such as vision and audition, are also engaged before an ingestive event. Sights, sounds, and smells can alert organisms to the presence of food as well as inform the organism as to the specifics of which taste(s) to expect. As such, the neurophysiology of taste is necessarily intertwined with that of other senses and with that of cognitive and homeostatic systems.
Andrew J. King
Information processing in the auditory system shows considerable adaptive plasticity across different timescales. This ranges from very rapid changes in neuronal response properties—on the order of hundreds of milliseconds when the statistics of sounds vary or seconds to minutes when their behavioral relevance is altered—to more gradual changes that are shaped by experience and learning. Many aspects of auditory processing and perception are sculpted by sensory experience during sensitive or critical periods of development. This developmental plasticity underpins the acquisition of language and musical skills, matches neural representations in the brain to the statistics of the acoustic environment, and enables the neural circuits underlying the ability to localize sound to be calibrated by the acoustic consequences of growth-related changes in the anatomy of the body. Although the length of these critical periods depends on the aspect of auditory processing under consideration, varies across species and brain level, and may be extended by experience and other factors, it is generally accepted that the potential for plasticity declines with age. Nevertheless, a substantial degree of plasticity is exhibited in adulthood. This is important for the acquisition of new perceptual skills; facilitates improvements in the detection or discrimination of fine differences in sound properties; and enables the brain to compensate for changes in inputs, including those resulting from hearing loss. In contrast to the plasticity that shapes the developing brain, perceptual learning normally requires the sound attribute in question to be behaviorally relevant and is driven by practice or training on specific tasks. Progress has recently been made in identifying the brain circuits involved and the role of neuromodulators in controlling plasticity, and an understanding of plasticity in the central auditory system is playing an increasingly important role in the treatment of hearing disorders.