老化对猴中颞视区细胞方向选择性的影响
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摘要
老化使视觉的正常功能受到严重的削弱。但是眼睛的光学系统老年性改变并不能完全解释很多视觉功能损伤。通常认为神经系统的退化是这种老年性视觉功能降低的主要原因。在过去的几年内,很多研究组发现老年动物视觉皮层细胞的一系列反应特性发生了改变,例如:老年猕猴初级视皮层、次级视皮层细胞的方位方向选择性显著性降低。这些在细胞水平上的变化被认为是老年性视觉功能损伤的神经机制。为了更全面的了解正常老化对视觉皮层细胞功能的影响,本研究采用在体细胞外单位记录方法,从以下两方面进一步比较青年猕猴和老年猕猴视觉皮层细胞反应特性的差异:
1.中颞视区(MT)细胞方向选择性的功能衰退
精确感知物体的运动方向和速度的能力对于生存是至关重要的。近年来的许多心理物理学实验表明人们的这种能力在正常老化过程中发生了衰退。但是这种衰退不能完全由眼视光和视网膜的变化来解释。因此,Spear提出假说认为这种衰退来源于视觉中枢的功能性退化。
关于这种视觉功能的衰退机制使用细胞外记录的方法已经在几个不同的脑区进行了研究。这些研究结果表明老化对外膝体的影响很小,而对V1(PrimaryVisual Cortex、初级视皮层)和V2(Secondary Viusal Cortex、次级视皮层)区的影响比较严重。这些研究表明V1和V2区细胞的方向方位选择性在老化过程中显著退化。同时还发现V2区细胞的方位选择性受老化的影响比V1区的严重。而且过度活动和信噪比降低伴随着这种细胞的退化。过度活动和选择性的降低被认为是由GABA介导的抑制系统衰退导致的。
众所周知,方向选择性细胞在运动处理的过程中起着非常重要的作用。在运动处理早期主要有V1区细胞起作用。V1区运动敏感细胞的最优运动方向与该细胞最优方位正交,因此学者普遍认为V1细胞对运动刺激的组分进行反应。近来的实验表明老化降低了V1细胞的方向选择性。但是到目前为止,老化对运动处理后期的影响尚不知道。
中颞视区(Middle Temporal area、MT)和高阶的运动检测处理密切相关。在这个区域,90%以上的细胞都有很强的方向选择性。这些选择性细胞的一部分是PDS细胞(Pattern direction selective cell or pattern cell),他们能检测物体的运动方向。由于这类细胞也存在于人类的MT+区。所以,研究老化对中颢视区细胞,特别是PDS细胞反应特性的影响有着非常重要的意义。为了探讨老化对运动处理后期的影响及其和行为的关系,本实验研究了老化对猕猴的中颢视区(MT)细胞功能的影响。我们还研究了老化对PDS细胞的比例和V1、MT区的方向选择性的影响。结果表明,与青年猕猴的MT细胞相比,老年猕猴的MT细胞方向选择性显著性降低。通过定量和统计的方法比较老化对MT细胞和V1细胞的方向选择性的影响,我们发现MT细胞受老化影响更严重。我们还发现老年猕猴中颢视区的PDS细胞所占的比例显著性下降。这种年龄相关的变化伴随着诱发发放升高、自发发放升高和信噪比降低。总之,我们的实验结果表明年龄依赖的功能性衰退发生在MT和V1区。这种功能性衰退可能导致了正常老化过程中视运动知觉的衰退。
2.老年猕猴V1区皮层内的方位方向选择性的衰退
普遍认为灵长类视觉系统分为两个通路,负责物体识别的背侧通路(又称M通路)和负责空间识别和运动知觉的腹侧通路(又称P通路),M通路和P通路并行处理,而各个通路内的信息处理却是逐级的,级别比较高的脑区执行比较复杂的功能。
在过去的十多年里,有不少研究是使用单细胞记录技术在不同的脑区探讨年龄相关的老化机制。这些研究表明老化对外膝体的影响极小。而在初级视皮层,细胞的方位、方向和对比敏感度都发生了衰退。在V2区的研究表明,V2区细胞的方位选择性的衰退比V1区严重。在MT区的研究也表明,MT细胞的方向选择性和对比敏感度受老化的影响也比V1严重。这种影响从LGN、V1到V2和MT的视觉通路上是逐级增加的。这些实验似乎揭示着一个假设:老化对视觉通路的影响是逐级累积的,即级别越高的脑区功能受老化的影响越严重。
视觉信息除了脑区之间的功能级别不同外,在脑区内部的功能级别也是不同的。目前研究比较多的是初级视皮层的皮层内功能层级结构。如果前述提出的假设成立的话,我们应该发现复杂细胞的反应特性受老化的影响比简单细胞严重。因此,我们使用在体单细胞记录的方法在麻醉麻痹猕猴上研究这个问题。
结果发现与青年猕猴相比,老年猕猴简单细胞的方位方向选择性虽然有轻微降低,但是没有达到统计显著性。而复杂细胞的方位方向选择性显著性降低。也就是说简单细胞和复杂细胞受老化影响的程度不同。这表明在正常老化过程中初级视皮层皮层内的高级功能受老化的影响更为严重。这给我们的假设提供了进一步的支持。
通过上述的两个实验,我们研究了猕猴视皮层细胞老年性功能退化在不同的脑区和不同功能层级的表现特点。结果发现老年猕猴MT细胞的功能,方向选择性,显著性降低,并且比V1细胞的改变更为明显。而且,其中和图像连续性运动感知行为密切相关的一类MT细胞——PDS细胞发生了丢失。MT区细胞发生的老年性功能衰退可能导致了老年人视运动知觉的损伤。另外,我们认为功能级别越高的脑区功能可能受老化的影响更严重。通过研究老化对简单细胞和复杂细胞方位方向选择性的影响,所得结果进一步支持了我们的这个想法。
Visual functions are impaired significantly by aging.The aging-related visual deficits can be observed even after the optical factor has been well controlled.It is suggested that the central nerve system plays an important role in generation of such deficits.In the past two decades,several alterations in response properties of visual cortical cells have been reported in senescent animal models,which were considered as the neural mechanisms underlying the aging-related degradation of vision.In order to a more comprehensive understanding about the aging effects on visual cortices and the relationship between the changes at cellular level and the functional degeneration at the whole system level,in the present study,we used in vivo extracellular single-unit recording techniques to compare the response property of visual cortical cells in young and old monkeys.The study included 2 experiments:
1.Aging affects the direction selectivity of MT cells in rhesus monkeys.
The ability to accurately perceive the direction and speed of moving objects is critical for survival.Many psychophysical studies have shown that this ability declines in humans during normal aging.This cannot be due to optical changes or changes in the retina alone.Therefore,it has been hypothesized that this decline results from functional degradation in central visual areas.
The mechanisms that underlie the visual decline that accompanies aging have been investigated using single-cell recording techniques in different visual areas. Studies have provided evidence that the effects of aging on the dorsal lateral geniculate nucleus(dLGN) are minor,while those in the striate cortex(V1) and extrastriate cortex(V2) are severe.Both the orientation and direction selectivity of V1 and V2 cells degrade during senescence.These declines are accompanied by hyperactivity and decreased signal-to-noise ratios.Such hyperactivity and decreased selectivity are thought to be due to the degradation of GABA-mediated inhibition within the visual cortex.
It is known that direction-selective neurons play an important role in motion processing.V1 cells are involved in early stages of motion perception. Motion-sensitive neurons in this area respond to the 'component' motion of moving stimuli.These cells signal motion that is orthogonal to their preferred orientations. Recent studies have shown that aging reduces the direction selectivity of V1 cells.To date,nothing is known about age-related changes in later stages of motion processing.
The middle temporal area(MT or V5) of the extrastriate cortex has been linked to higher order motion detection.In this area,more than 90%of the neurons are direction-selective.A proportion of MT direction-selective neurons are pattern cells. These cells can detect the direction of moving objects independently of their particular spatial pattern.Thus,the responses of these cells can be equated with human perception.In fact,a population of pattern cells exists in human MT+,and the activity of these neurons is closely linked to the perception of coherent pattern motion.
We studied the effect of aging upon MT cells in macaque monkeys by comparing the proportion of pattern cells and the degree of direction selectivity of MT cells in young and old monkeys.The results show that the proportion of pattern cells in MT decreases in old macaques.A comparison of direction selectivity of areas V1 and MT in old and young monkeys provides evidence that DB in cells in both areas decrease in old monkeys.MT cells showed a larger decrease than V1 cells did.These age-related changes were accompanied by increases in peak response and spontaneous activity,as well as a decrease in signal-to-noise ratio.Taken together,our results indicate that functional degradation occurs in both areas of MT and V1 during normal aging,and that area MT is affected by aging more severely than the striate cortex is. Such functional degradation in area MT may contribute to the decline in perception of moving objects during normal aging.
2.Degradation of intra-cortical processing in primary visual cortex of senescent monkey.
The primate visual system is broadly organized into two segregated processing pathways,a ventral stream for object vision and a dorsal stream for space vision, termed as P pathway and M pathway.Within both streams,visual information is processed sequentially such that progressively more complex functions are carried out at progressively higher levels in the hierarchy.
Over the past decades,the mechanisms underlying visual declines that accompany aging have been investigated using single-cell recording technique in a variety of visual areas and deficits in neuronal response was found,with different extends,along the visual hierarchy.The emerged picture suggested that the aging effect could be inserted into each processing stage and resulted in the progressive functional degradation along the hierarchy of visual information processing.For example,studies have provided evidence that the effects of aging on the dLGN are minor,while those in striate cortex are severe,In P pathway,extrastriate cortex(V2) is found more severe affects by aging than V1.Similarly,in M pathway,MT is also found to be affected more severe than V1.Taken these studies together,it is reasonable to hypothesize that higher hierarchical levels are affected by aging more severe.
Besides the visual hierarchy composed of different cortical structures or areas, there are similar hierarchies of processing within individual areas.The most well studied example is the simple cell and complex cell in V1.In 1959,Hubel and Wiesel first reported that in the striate cortex,neurons respond selectively to the orientation of local contours and to the direction of motion of a visual stimulus.Also,they found that those neurons could be classified into simple and complex cells based on their receptive field properties.According to hierarchical processing model proposed by Hubel and Wiesel,simple cells receiving inputs from dorsal lateral geniculate nucleus (dLGN) become selective to the orientation of a local contour in a specific location. Complex cells,which carry out more complex functions,integrating information from simple cells become selective to the orientation of a local contour regardless of its exact position within the receptive field.Therefore,the hypothesis that we want to test in the present study is:the complex cells,located at the higher stage of processing, affected by aging more severe than simple cells.To this end,we investigated the visual response of cortical cells in anesthetized and paralyzed monkeys.Orientation and direction selectivity of simple and complex cells between young and old monkeys were compared.
Our results have shown that the orientation and direction selectivities to stimuli of simple cells are relatively normal in old V1 area.However,the selectivities of complex cells decrease in old monkeys.The differential age-related changes of the two types of cells indicate that intra-cortical information processing suffers impairments in different degree during aging.
By these two experiments,we studied the different characteristics of aging effects in different brain areas and the degradation of information processing during normal aging.The results indicate that 1) there is more severe functional degradation of higher hierarchy;2) The degradation of MT cells in old monkeys might result in visual motion deficits in old human.3) The hypothesis that higher hierarchical levels are affected by aging more severe was well supported by our experiments and previous studies.
1.中颞视区(MT)细胞方向选择性的功能衰退
精确感知物体的运动方向和速度的能力对于生存是至关重要的。近年来的许多心理物理学实验表明人们的这种能力在正常老化过程中发生了衰退。但是这种衰退不能完全由眼视光和视网膜的变化来解释。因此,Spear提出假说认为这种衰退来源于视觉中枢的功能性退化。
关于这种视觉功能的衰退机制使用细胞外记录的方法已经在几个不同的脑区进行了研究。这些研究结果表明老化对外膝体的影响很小,而对V1(PrimaryVisual Cortex、初级视皮层)和V2(Secondary Viusal Cortex、次级视皮层)区的影响比较严重。这些研究表明V1和V2区细胞的方向方位选择性在老化过程中显著退化。同时还发现V2区细胞的方位选择性受老化的影响比V1区的严重。而且过度活动和信噪比降低伴随着这种细胞的退化。过度活动和选择性的降低被认为是由GABA介导的抑制系统衰退导致的。
众所周知,方向选择性细胞在运动处理的过程中起着非常重要的作用。在运动处理早期主要有V1区细胞起作用。V1区运动敏感细胞的最优运动方向与该细胞最优方位正交,因此学者普遍认为V1细胞对运动刺激的组分进行反应。近来的实验表明老化降低了V1细胞的方向选择性。但是到目前为止,老化对运动处理后期的影响尚不知道。
中颞视区(Middle Temporal area、MT)和高阶的运动检测处理密切相关。在这个区域,90%以上的细胞都有很强的方向选择性。这些选择性细胞的一部分是PDS细胞(Pattern direction selective cell or pattern cell),他们能检测物体的运动方向。由于这类细胞也存在于人类的MT+区。所以,研究老化对中颢视区细胞,特别是PDS细胞反应特性的影响有着非常重要的意义。为了探讨老化对运动处理后期的影响及其和行为的关系,本实验研究了老化对猕猴的中颢视区(MT)细胞功能的影响。我们还研究了老化对PDS细胞的比例和V1、MT区的方向选择性的影响。结果表明,与青年猕猴的MT细胞相比,老年猕猴的MT细胞方向选择性显著性降低。通过定量和统计的方法比较老化对MT细胞和V1细胞的方向选择性的影响,我们发现MT细胞受老化影响更严重。我们还发现老年猕猴中颢视区的PDS细胞所占的比例显著性下降。这种年龄相关的变化伴随着诱发发放升高、自发发放升高和信噪比降低。总之,我们的实验结果表明年龄依赖的功能性衰退发生在MT和V1区。这种功能性衰退可能导致了正常老化过程中视运动知觉的衰退。
2.老年猕猴V1区皮层内的方位方向选择性的衰退
普遍认为灵长类视觉系统分为两个通路,负责物体识别的背侧通路(又称M通路)和负责空间识别和运动知觉的腹侧通路(又称P通路),M通路和P通路并行处理,而各个通路内的信息处理却是逐级的,级别比较高的脑区执行比较复杂的功能。
在过去的十多年里,有不少研究是使用单细胞记录技术在不同的脑区探讨年龄相关的老化机制。这些研究表明老化对外膝体的影响极小。而在初级视皮层,细胞的方位、方向和对比敏感度都发生了衰退。在V2区的研究表明,V2区细胞的方位选择性的衰退比V1区严重。在MT区的研究也表明,MT细胞的方向选择性和对比敏感度受老化的影响也比V1严重。这种影响从LGN、V1到V2和MT的视觉通路上是逐级增加的。这些实验似乎揭示着一个假设:老化对视觉通路的影响是逐级累积的,即级别越高的脑区功能受老化的影响越严重。
视觉信息除了脑区之间的功能级别不同外,在脑区内部的功能级别也是不同的。目前研究比较多的是初级视皮层的皮层内功能层级结构。如果前述提出的假设成立的话,我们应该发现复杂细胞的反应特性受老化的影响比简单细胞严重。因此,我们使用在体单细胞记录的方法在麻醉麻痹猕猴上研究这个问题。
结果发现与青年猕猴相比,老年猕猴简单细胞的方位方向选择性虽然有轻微降低,但是没有达到统计显著性。而复杂细胞的方位方向选择性显著性降低。也就是说简单细胞和复杂细胞受老化影响的程度不同。这表明在正常老化过程中初级视皮层皮层内的高级功能受老化的影响更为严重。这给我们的假设提供了进一步的支持。
通过上述的两个实验,我们研究了猕猴视皮层细胞老年性功能退化在不同的脑区和不同功能层级的表现特点。结果发现老年猕猴MT细胞的功能,方向选择性,显著性降低,并且比V1细胞的改变更为明显。而且,其中和图像连续性运动感知行为密切相关的一类MT细胞——PDS细胞发生了丢失。MT区细胞发生的老年性功能衰退可能导致了老年人视运动知觉的损伤。另外,我们认为功能级别越高的脑区功能可能受老化的影响更严重。通过研究老化对简单细胞和复杂细胞方位方向选择性的影响,所得结果进一步支持了我们的这个想法。
Visual functions are impaired significantly by aging.The aging-related visual deficits can be observed even after the optical factor has been well controlled.It is suggested that the central nerve system plays an important role in generation of such deficits.In the past two decades,several alterations in response properties of visual cortical cells have been reported in senescent animal models,which were considered as the neural mechanisms underlying the aging-related degradation of vision.In order to a more comprehensive understanding about the aging effects on visual cortices and the relationship between the changes at cellular level and the functional degeneration at the whole system level,in the present study,we used in vivo extracellular single-unit recording techniques to compare the response property of visual cortical cells in young and old monkeys.The study included 2 experiments:
1.Aging affects the direction selectivity of MT cells in rhesus monkeys.
The ability to accurately perceive the direction and speed of moving objects is critical for survival.Many psychophysical studies have shown that this ability declines in humans during normal aging.This cannot be due to optical changes or changes in the retina alone.Therefore,it has been hypothesized that this decline results from functional degradation in central visual areas.
The mechanisms that underlie the visual decline that accompanies aging have been investigated using single-cell recording techniques in different visual areas. Studies have provided evidence that the effects of aging on the dorsal lateral geniculate nucleus(dLGN) are minor,while those in the striate cortex(V1) and extrastriate cortex(V2) are severe.Both the orientation and direction selectivity of V1 and V2 cells degrade during senescence.These declines are accompanied by hyperactivity and decreased signal-to-noise ratios.Such hyperactivity and decreased selectivity are thought to be due to the degradation of GABA-mediated inhibition within the visual cortex.
It is known that direction-selective neurons play an important role in motion processing.V1 cells are involved in early stages of motion perception. Motion-sensitive neurons in this area respond to the 'component' motion of moving stimuli.These cells signal motion that is orthogonal to their preferred orientations. Recent studies have shown that aging reduces the direction selectivity of V1 cells.To date,nothing is known about age-related changes in later stages of motion processing.
The middle temporal area(MT or V5) of the extrastriate cortex has been linked to higher order motion detection.In this area,more than 90%of the neurons are direction-selective.A proportion of MT direction-selective neurons are pattern cells. These cells can detect the direction of moving objects independently of their particular spatial pattern.Thus,the responses of these cells can be equated with human perception.In fact,a population of pattern cells exists in human MT+,and the activity of these neurons is closely linked to the perception of coherent pattern motion.
We studied the effect of aging upon MT cells in macaque monkeys by comparing the proportion of pattern cells and the degree of direction selectivity of MT cells in young and old monkeys.The results show that the proportion of pattern cells in MT decreases in old macaques.A comparison of direction selectivity of areas V1 and MT in old and young monkeys provides evidence that DB in cells in both areas decrease in old monkeys.MT cells showed a larger decrease than V1 cells did.These age-related changes were accompanied by increases in peak response and spontaneous activity,as well as a decrease in signal-to-noise ratio.Taken together,our results indicate that functional degradation occurs in both areas of MT and V1 during normal aging,and that area MT is affected by aging more severely than the striate cortex is. Such functional degradation in area MT may contribute to the decline in perception of moving objects during normal aging.
2.Degradation of intra-cortical processing in primary visual cortex of senescent monkey.
The primate visual system is broadly organized into two segregated processing pathways,a ventral stream for object vision and a dorsal stream for space vision, termed as P pathway and M pathway.Within both streams,visual information is processed sequentially such that progressively more complex functions are carried out at progressively higher levels in the hierarchy.
Over the past decades,the mechanisms underlying visual declines that accompany aging have been investigated using single-cell recording technique in a variety of visual areas and deficits in neuronal response was found,with different extends,along the visual hierarchy.The emerged picture suggested that the aging effect could be inserted into each processing stage and resulted in the progressive functional degradation along the hierarchy of visual information processing.For example,studies have provided evidence that the effects of aging on the dLGN are minor,while those in striate cortex are severe,In P pathway,extrastriate cortex(V2) is found more severe affects by aging than V1.Similarly,in M pathway,MT is also found to be affected more severe than V1.Taken these studies together,it is reasonable to hypothesize that higher hierarchical levels are affected by aging more severe.
Besides the visual hierarchy composed of different cortical structures or areas, there are similar hierarchies of processing within individual areas.The most well studied example is the simple cell and complex cell in V1.In 1959,Hubel and Wiesel first reported that in the striate cortex,neurons respond selectively to the orientation of local contours and to the direction of motion of a visual stimulus.Also,they found that those neurons could be classified into simple and complex cells based on their receptive field properties.According to hierarchical processing model proposed by Hubel and Wiesel,simple cells receiving inputs from dorsal lateral geniculate nucleus (dLGN) become selective to the orientation of a local contour in a specific location. Complex cells,which carry out more complex functions,integrating information from simple cells become selective to the orientation of a local contour regardless of its exact position within the receptive field.Therefore,the hypothesis that we want to test in the present study is:the complex cells,located at the higher stage of processing, affected by aging more severe than simple cells.To this end,we investigated the visual response of cortical cells in anesthetized and paralyzed monkeys.Orientation and direction selectivity of simple and complex cells between young and old monkeys were compared.
Our results have shown that the orientation and direction selectivities to stimuli of simple cells are relatively normal in old V1 area.However,the selectivities of complex cells decrease in old monkeys.The differential age-related changes of the two types of cells indicate that intra-cortical information processing suffers impairments in different degree during aging.
By these two experiments,we studied the different characteristics of aging effects in different brain areas and the degradation of information processing during normal aging.The results indicate that 1) there is more severe functional degradation of higher hierarchy;2) The degradation of MT cells in old monkeys might result in visual motion deficits in old human.3) The hypothesis that higher hierarchical levels are affected by aging more severe was well supported by our experiments and previous studies.
引文
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