The organization and physiology of the auditory thalamus and its role in processing acoustic features important for speech perception
Introduction
Much of the research focus on the sensory and cognitive aspects of language centers on cortical activities. The cerebral cortex, however, is inextricably linked to the collection of forebrain nuclei known as the thalamus. Thalamocortical pathways dictate the sensory and higher-order representations in cortex while corticothalamic pathways generate dynamic, context-dependent changes in thalamic responsiveness to form an iterative signaling loop. This review will describe the functional organization of the auditory thalamus as it relates to the representation of sound features that are relevant for speech perception.
The thalamus is a collection of nuclei whose main and best-studied projections are to the cerebral cortex, comprising projections to all areas of cortex. The main auditory-responsive portion of the thalamus is called the medial geniculate body (MGB), and it is the information bottleneck for neural representations of sounds being sent to auditory cortex.
Whereas early views of the thalamus were that it served as a simple ‘relay’ or ‘gateway’ to the cortex, numerous studies have demonstrated that thalamic neurons transform their inputs en route to their cortical or subcortical targets (Hubel and Wiesel, 1961, Sherman and Guillery, 2002). As we will show, the MGB actively and dynamically shapes the auditory representations that reach the cerebral cortex. Rather than acting as a simple conduit for incoming auditory representations, the MGB acts like a funhouse mirror in the sense that it can filter and distort incoming inputs to enhance representation and perception of acoustic features for use by the auditory cortex (AC).
Section snippets
Acoustic characteristics of the speech signal relevant for auditory processing and receptive language
Human speech and animal vocalizations have complex sound characteristics that must be represented accurately by neural populations in order to recognize, understand, and converse with individuals in a variety of sound backgrounds and in the presence of multiple speakers. For speech, this includes not only the ability to identify the words that are spoken, but also the identity and gender of the speaker as well as the emotional content of their speech. Unlike the tones often used to probe
Overview of the anatomical and functional organization of the MGB
The MGB can be divided into three broad subdivisions, whose organization and properties are summarized in Table 1 and whose spatial arrangement can be seen in Fig. 1, going from rostral to caudal, using the marmoset as an example. The ventral division of the MGB (MGV) is the “core” subdivision for the rapid transmission of auditory information that is sharply tuned for frequency and able to respond to fast temporal modulations of sounds. For primates, this pathway also includes the anterodorsal
Connectivity of the MGB-feedforward afferents
Across species, auditory inputs to the MGV arise mainly from the ipsilateral central nucleus of the IC (ICC, Fig. 2) (Calford and Aitkin, 1983, Gonzalez-Hernandez et al., 1991, LeDoux et al., 1985, Oliver and Hall, 1978, Rouiller and de Ribaupierre, 1985). At the light microscopic level, many ICC axons ended as large terminals in MGV that are grouped within 50–100 μm of each other (Bartlett et al., 2000, Malmierca et al., 1997, Pallas and Sur, 1994), so that they may contact the dendritic arbors
Connectivity of the MGB-efferents
Summarizing recent reviews (e.g. Lee, 2012, Winer et al., 2005), thalamocortical axons from MGV terminate mainly in cortical layers 3 and 4 of core auditory cortex. En route to layer 3/4, MGV axons emit collaterals that terminate in the auditory portion of the thalamic reticular nucleus (TRN) (Fig. 2) (Ojima, 1994). Within the MGV, there is some segregation in the regions that give rise to projections to different core auditory cortical regions (Read, Nauen, et al., 2011), such that the caudal
Connectivity of the MGB-feedback afferents
The basic organization of cortical feedback to MGB has been well-studied (see Lee et al., 2004, Lee, 2012 for reviews). Primary auditory cortex is broadly reciprocally connected with MGV (Fig. 4A), such that regions in MGV that project to a given area of auditory cortex are likely to receive significant corticothalamic feedback from layer 6 neurons of that area of cortex (Kimura et al., 2005, Llano and Sherman, 2008, Winer et al., 2001). Similar reciprocity holds for corticothalamic MGD and CPL
Responses to tone stimuli – frequency tuning
Accurate neural representations of frequencies are critical for accurate perceptions of speech sounds (Carroll and Zeng, 2007, Glasberg and Moore, 1989), such as for discriminating between vowel formants, between speakers, and identifying gender. This is particularly true for speech reception in background noise (Glasberg and Moore, 1989, Horst, 1987), for hearing impaired listeners (Carroll et al., 2011, Glasberg and Moore, 1989) and for listeners with specific language impairment (Hill et
Responses to tone stimuli – sound level tuning
As discussed in the previous section, frequency selectivity can change as a function of sound level. This is even the case for a tone or narrow-band noise centered at a neuron’s best frequency. It can also affect how time-varying changes in modulation frequency and modulation depth are represented, particularly for relatively slow temporal modulations (<10 Hz, Malone, Scott, & Semple, 2007). That is, the ability to detect and discriminate slow temporal modulations, which is important in speech
Responses to monaural and binaural stimulation and sound localization cues
In an auditory scene with multiple sources, spatial localization is a major cue for separating those sources (Drennan et al., 2000; Schimmel, van de Par, Breebaart, & Kohlrausch, 2008). Studies in the cat indicate that about 60% of MGB neurons can be excited by stimuli to either ear, but 20–30% can be excited only by contralateral ear stimulation (Calford, 1983). About 10–20% are inhibited by ipsilateral stimulation, although few are only inhibited without excitation (Calford, 1983). Many MGB
Temporal processing in the MGB
Most sound stimuli exhibit temporal modulations that are important for identifying and discriminating those sounds. Earlier, the idea of three different ranges of temporal modulations was introduced; 1–50 Hz for rudimentary speech recognition, mainly in quiet conditions, 50–500 Hz for speaker, gender and emotion identification, and >500 Hz for additional cues for speaker and emotion identification. Furthermore, modulations >50 Hz aid with understanding speech in noise.
For simple temporally
Cellular bases for temporal processing – intrinsic properties of MGB neurons
In thinking about how animals and people perceive, process, and respond to sounds, it is important to understand that these complex, macroscopic processes occur due to a myriad of cellular and subcellular interactions between neurons in the auditory pathways. One way that MGB neurons may regulate how their responses to synaptic input are processed is through their membrane properties and intrinsic conductances, which can produce tradeoffs in sensitivity and fidelity.
It is necessary to measure
Cellular bases for temporal processing – synaptic properties of MGB neurons
It is clear from the previous sections that MGB neurons in different subdivisions represent sound stimuli quite differently. Between MGV and MGD neurons, there are differences in connectivity and cell morphology, but only minor differences in intrinsic properties. Therefore, significant differences in auditory responses are likely to originate mainly from the inherited tuning of their inputs and the way that afferent spike trains are transformed by the synapses. Previous studies of the IC input
MGB responses to vocalizations
Vocalizations are an important class of stimuli to examine for their neural representations, because they combine a high acoustic complexity with behavioral relevance. Human fMRI studies have shown significant speech-related modulation of MGB BOLD activity that is correlated with discriminating speech between different speakers (von Kriegstein, Patterson, & Griffiths, 2008) and speaker emotion (Ethofer et al., 2012). Neurons in the awake guinea pig and monkey MGB have been shown to respond to
MGB-effects of cortical and TRN feedback
Perception of sounds results not from the simple decomposition and transmission of sound features, but it is actively constructed by the interplay of ascending sensory input, intracortical processing, and feedback processing from auditory cortex to thalamus and other subcortical structures. MGB responses to acoustic stimuli are typically attributed to excitation by IC axons, but studies have indicated that corticothalamic feedback can alter MGB responses (Zhang, Suga, & Yan, 1997). This may be
Modulation of MGD and MGM/SG responses by adaptation, reward and non-auditory stimuli
The basic finding from multiple studies is that MGV neurons generally do not exhibit long-term changes in their receptive field properties and are not strongly influenced by non-auditory inputs or reward (Edeline and Weinberger, 1991a, Komura et al., 2005, Komura et al., 2001). This makes sense if a main function of MGV is to provide auditory cortex with a reliable, context-independent representation of auditory stimuli. By contrast, MGD, SG, and MGM neurons have responses that are strongly
Changes in thalamic structure and function in neurological disorders
The primary roles of thalamocortical neurons, especially in the sensory pathways, are to control which information reaches the cerebral cortex and to shape the neural representations of that information. Similar to most brain regions, overall, there are very few physiological recordings of MGB in humans, so nearly all estimates of MGB neural representations in humans arise from non-invasive methods such as mid-latency auditory evoked potentials and fMRI. Activation of the MGB (fMRI BOLD signal)
FOXP2 and MGB
FOXP2 is a transcription factor whose proper function is critical for speech, language and other natural communication in humans, rodents, and birds. Mutations in FOXP2 lead to deficits both in speech production and linguistic perceptual processing in humans (Lai, Gerrelli, Monaco, Fisher, & Copp, 2003), aberrant vocalizations in mice (Fujita et al., 2008), and impairments in auditory learning (Kurt, Fisher, & Ehret, 2012). In mammals, FOXP2 is enriched in the auditory thalamus (MGB), deep
Schizophrenia
Consistent with its role in dynamically filtering auditory input to the cerebral cortex, the MGB responds differently in schizophrenics versus non-schizophrenics. Many schizophrenics have difficulties ignoring competing sounds to focus on a target sound. In one study, urban noise consisting of multitalker speech, music, and other sounds produced a hyperactivation of MGB and prefrontal cortex blood oxygenation level dependent (BOLD) functional magnetic resonance imaging (fMRI) responses (
Dyslexia
Dyslexics have reading difficulties, often coupled with auditory and other sensory deficits (Fitch et al., 1994, Goswami et al., 2002, Shaywitz and Shaywitz, 2005). A recent fMRI study found that impairments in phonological processing were correlated with deficiencies in MGB activation and with reading scores (Díaz, Hintz, Kiebel, & von Kriegstein, 2012). Auditory and reading deficits observed in people with dyslexia have been correlated with anatomical abnormalities in the MGB (Galaburda et
Alzheimer’s disease
An early predictor of cognitive decline in Alzheimer’s disease is the presence of central auditory deficits, especially for complex signals such as speech in noise (Gates, Beiser, Rees, D’Agostino, & Wolf, 2002). There are changes in the IC and MGB even before the presence of the standard neuropathological markers of neurofibrillary tangles made of tau protein or senile plaques made of beta-amyloid protein (Baloyannis, 2009). When Golgi-labeling was used to label the neurons from recently
Conclusions
Speech perception involves complex, rapid and precise neural representations of relevant features such as spectral peaks, modulations on multiple timescales, contrast from noise, location of sound sources, and relationships to other sensory features and behavioral context. The MGB participates in the active shaping of these neural representations that then go to auditory cortex and to subcortical targets to shape our perceptions. MGB neurons do not act as a simple gate that may be open or shut
Acknowledgments
Dr. Xiaoqin Wang provided facilities and mentorship for some of the work described here. Some work reported in this review was funded by NIDCD grants DC-006357 (ELB) and DC-003180 and DC-005808 (XQW). Past and current work by Dr. Bartlett has been generously funded by the Hearing Health Foundation.
References (227)
- et al.
A possible role for a paralemniscal auditory pathway in the coding of slow temporal information
Hearing Research
(2011) - et al.
Identification of subdivisions in the medial geniculate body of the guinea pig
Hearing Research
(2007) - et al.
Physiological differences between histologically defined subdivisions in the mouse auditory thalamus
Hearing Research
(2011) - et al.
Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex
Hearing Research
(1995) Dendritic pathology in Alzheimer’s disease
Journal of the Neurological Sciences
(2009)- et al.
Effects of paired-pulse and repetitive stimulation on neurons in the rat medial geniculate body
Neuroscience
(2002) - et al.
Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body
Neuroscience
(2000) - et al.
Fundamental frequency discrimination and speech perception in noise in cochlear implant simulations
Hearing Research
(2007) - et al.
Parvalbumin and calbindin are differentially distributed within primary and secondary subregions of the mouse auditory forebrain
Neuroscience
(2001) - et al.
Do auditory responses recorded from awake animals reflect the anatomical parcellation of the auditory thalamus?
Hearing Research
(1999)
Regional variations of noise-induced changes in operating range in cat AI
Hearing Research
Early cortical damage in rat somatosensory cortex alters acoustic feature representation in primary auditory cortex
Neuroscience
Auditory evoked potentials in a patient with a unilateral lesion of the inferior colliculus and medial geniculate body
Electroencephalography and Clinical Neurophysiology
Single unit activity in the auditory cortex and the medial geniculate body of the rhesus monkey: Behavioral modulation
Brain Research
Divergent projections of projecting neurons of the inferior colliculus to the medial geniculate body and the contralateral inferior colliculus in the rat
Hearing Research
Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: Differential distribution and cortical layer specific projections
Brain Research
Neural correlates of cubic difference tones in the medial geniculate body of the cat
Hearing Research
Click-evoked response patterns of single units in the medial geniculate body of the cat
Journal of Neurophysiology
Medial geniculate body: Unit responses in the awake cat
Journal of Neurophysiology
Rate-level functions of neurons in the inferior colliculus of cats measured with the use of free-field sound stimuli
Journal of Neurophysiology
Responses of single cells in the medial geniculate body of awake squirrel monkeys
Experimental Brain Research
Fiber projections of the superior colliculus in the cat
Journal of Comparative Neurology
The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat
Journal of Comparative Neurology
Evidence for a direct, short latency projection from the dorsal cochlear nucleus to the auditory thalamus in the guinea pig
European Journal of Neuroscience
Stimulus-specific adaptation occurs in the auditory thalamus
Journal of Neuroscience
Ventral temporal cortex in the rat: Connections of secondary auditory areas Te2 and Te3
Journal of Comparative Neurology
Stimulus-specific adaptation in the auditory thalamus of the anesthetized rat
PLoS ONE
Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus in the rat
Journal of Comparative Neurology
Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body
Journal of Neurophysiology
Neural representations of temporally modulated signals in the auditory thalamus of awake primates
Journal of Neurophysiology
Representation of amplitude modulation envelope in the marmoset auditory thalamus
Society for Neuroscince Abs
Correlation of neural response properties with auditory thalamus subdivisions in the awake marmoset
Journal of Neurophysiology
Frequency transposition around dead regions simulated with a noiseband vocoder
Journal of the Acoustical Society of America
Stimulus-specific adaptation in the gerbil primary auditory thalamus is the result of a fast frequency-specific habituation and is regulated by the corticofugal system
Journal of Neuroscience
Neural response properties of primary, rostral, and rostrotemporal core fields in the auditory cortex of marmoset monkeys
Journal of Neurophysiology
The termination of spinomesencephalic fibers in cat: An experimental anatomical study
Anatomy & Embryology
Ultra-fine frequency tuning revealed in single neurons of human auditory cortex
Nature
Response properties of single units in areas of rat auditory thalamus that project to the amygdala. I. Acoustic discharge patterns and frequency receptive fields
Experimental Brain Research
The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units
Journal of Neuroscience
Ascending projections to the medial geniculate body of the cat: Evidence for multiple, parallel auditory pathways through thalamus
Journal of Neuroscience
Conservation and diversity of Foxp2 expression in muroid rodents: Functional implications
Journal of Comparative Neurology
Connections of some auditory-responsive posterior thalamic nuclei putatively involved in activation of the hypothalamo-pituitary-adrenocortical axis in response to audiogenic stress in rats: An anterograde and retrograde tract tracing study combined with Fos expression
Journal of Comparative Neurology
Fundamental frequency is critical to speech perception in noise in combined acoustic and electric hearing
Journal of the Acoustical Society of America
Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo
Journal of Physiology
Comparison of noise and tone azimuth tuning of neurons in cat primary auditory cortex and medical geniculate body
Journal of Neurophysiology
Impaired processing of complex auditory stimuli in rats with induced cerebrocortical microgyria: An animal model of developmental language disabilities
Journal of Cognitive Neuroscience
Sources of projections to subdivisions of the inferior colliculus in the rat
Journal of Comparative Neurology
Organization in the auditory sector of the cat’s thalamic reticular nucleus
Journal of Comparative Neurology
Cited by (77)
Several ways to wake you up by the thalamus
2023, NeuronThe human auditory system and audio
2023, Applied AcousticsNeural substrates of perception in the vestibular thalamus during natural self-motion: A review
2023, Current Research in Neurobiology